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Author Posting. © American Geophysical Union, 2005. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Journal of Geophysical Research 110 (2005): C09S16, doi:10.1029/2004JC002601. Comparison of eight iron experiments shows that maximum Chl a, the maximum DIC removal, and the overall DIC/Fe efficiency all scale inversely with depth of the wind mixed layer (WML) defining the light environment. Moreover, lateral patch dilution, sea surface irradiance, temperature, and grazing play additional roles. The Southern Ocean experiments were most influenced by very deep WMLs. In contrast, light conditions were most favorable during SEEDS and SERIES as well as during IronEx-2. The two extreme experiments, EisenEx and SEEDS, can be linked via EisenEx bottle incubations with shallower simulated WML depth. Large diatoms always benefit the most from Fe addition, where a remarkably small group of thriving diatom species is dominated by universal response of Pseudo-nitzschia spp. Significant response of these moderate (10–30 μm), medium (30–60 μm), and large (>60 μm) diatoms is consistent with growth physiology determined for single species in natural seawater. The minimum level of “dissolved” Fe (filtrate < 0.2 μm) maintained during an experiment determines the dominant diatom size class. However, this is further complicated by continuous transfer of original truly dissolved reduced Fe(II) into the colloidal pool, which may constitute some 75% of the “dissolved” pool. Depth integration of carbon inventory changes partly compensates the adverse effects of a deep WML due to its greater integration depths, decreasing the differences in responses between the eight experiments. About half of depth-integrated overall primary productivity is reflected in a decrease of DIC. The overall C/Fe efficiency of DIC uptake is DIC/Fe ∼ 5600 for all eight experiments. The increase of particulate organic carbon is about a quarter of the primary production, suggesting food web losses for the other three quarters. Replenishment of DIC by air/sea exchange tends to be a minor few percent of primary CO2 fixation but will continue well after observations have stopped. Export of carbon into deeper waters is difficult to assess and is until now firmly proven and quite modest in only two experiments. This research was supported by the European Union through programs CARUSO (1998– 2001), IRONAGES (1999 –2003), and COMET (2000–2003); the Netherlands- Bremen Oceanography program NEBROC-1; and the Netherlands Organization for Research NWO through the Netherlands Antarctic Program project FePath. Both the U.S. National Science Foundation and the U.S. Department of Energy provided significant support for the SOFeX program. M.R.L. acknowledges the U.S. National Science Foundation for support of IronEx and SOFeX projects and related studies (OCE-9912230, -9911765, and -0322074).
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Synthesis of iron fertilization experiments: From the Iron Age in the
Age of Enlightenment
Hein J. W. de Baar,
Philip W. Boyd,
Kenneth H. Coale,
Michael R. Landry,
Atsushi Tsuda,
Philipp Assmy,
Dorothee C. E. Bakker,
Yann Bozec,
Richard T. Barber,
Mark A. Brzezinski,
Ken O. Buesseler,
Marie Boye´,
Peter L. Croot,
Frank Gervais,
Maxim Y. Gorbunov,
Paul J. Harrison,
William T. Hiscock,
Patrick Laan,
Christiane Lancelot,
Cliff S. Law,
Maurice Levasseur,
Adrian Marchetti,
Frank J. Millero,
Jun Nishioka,
Yukihiro Nojiri,
Tim van Oijen,
Ulf Riebesell,
Micha J. A. Rijkenberg,
Hiroaki Saito,
Shigenobu Takeda,
Klaas R. Timmermans,
Marcel J. W. Veldhuis,
Anya M. Waite,
and Chi-Shing Wong
Received 16 July 2004; revised 8 May 2005; accepted 14 July 2005; published 28 September 2005.
[1]Comparison of eight iron experiments shows that maximum Chl a, the maximum DIC
removal, and the overall DIC/Fe efficiency all scale inversely with depth of the wind
mixed layer (WML) defining the light environment. Moreover, lateral patch dilution, sea
surface irradiance, temperature, and grazing play additional roles. The Southern Ocean
experiments were most influenced by very deep WMLs. In contrast, light conditions were
most favorable during SEEDS and SERIES as well as during IronEx-2. The two extreme
experiments, EisenEx and SEEDS, can be linked via EisenEx bottle incubations with
shallower simulated WML depth. Large diatoms always benefit the most from Fe addition,
where a remarkably small group of thriving diatom species is dominated by universal
response of Pseudo-nitzschia spp. Significant response of these moderate (10 30 mm),
medium (30–60 mm), and large (>60 mm) diatoms is consistent with growth physiology
determined for single species in natural seawater. The minimum level of ‘‘dissolved’’ Fe
(filtrate < 0.2 mm) maintained during an experiment determines the dominant diatom size
class. However, this is further complicated by continuous transfer of original truly
dissolved reduced Fe(II) into the colloidal pool, which may constitute some 75% of the
‘dissolved’’ pool. Depth integration of carbon inventory changes partly compensates the
adverse effects of a deep WML due to its greater integration depths, decreasing the
JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 110, C09S16, doi:10.1029/2004JC002601, 2005
Royal Netherlands Institute for Sea Research, Isle of Texel,
Marine Biology, University of Groningen, Haren, Netherlands.
National Institute of Water and Atmospheric Research, Centre for
Chemical and Physical Oceanography, Department of Chemistry, Uni-
versity of Otago, Dunedin, New Zealand.
Moss Landing Marine Laboratories, Moss Landing, California, USA.
Scripps Institution of Oceanography, University of California, San
Diego, La Jolla, California, USA.
Ocean Research Institute, University of Tokyo, Tokyo, Japan.
Alfred Wegener Institute for Polar and Marine Research, Bremerhaven,
School of Environmental Sciences, University of East Anglia,
Norwich, UK.
Nicholas School of the Environment and Earth Sciences, Duke
University, Beaufort, North Carolina, USA.
Marine Science Institute and Department of Ecology, Evolution, and
Marine Biology, University of California, Santa Barbara, Santa Barbara,
California, USA.
Woods Hole Oceanographic Institution, Woods Hole, Massachusetts,
Universite´ de Bretagne Occidentale, Brest, France.
Copyright 2005 by the American Geophysical Union.
Leibniz Institut fu¨r Meereswissenschaften, IFM-GEOMAR, Kiel,
Institute of Marine and Coastal Sciences, Rutgers University, New
Brunswick, New Jersey, USA.
Atmospheric, Marine and Coastal Environment Program, Hong Kong
University of Science and Technology, Hong Kong, China.
Rosenstiel School of Marine and Atmospheric Science, University of
Miami, Miami, Florida, USA.
Ecologie des Systemes Aquatiques, Universite´ Libre de Bruxelles,
Brussels, Belgium.
National Institute of Water and Atmospheric Research, Wellington,
New Zealand.
De´partement de Biologie (Que´bec-Oce´ an), Universite´ Laval, Quebec,
University of British Columbia, Vancouver, British Columbia,
Central Research Institute of Electric Power Industry, Chiba, Japan.
National Institute for Environmental Studies, Tsukuba, Ibaraki, Japan.
Tohoku National Fisheries Research Institute, Miyagi, Japan.
Department of Aquatic Bioscience, University of Tokyo, Tokyo,
Centre for Water Research, University of Western Australia, Crawley,
Institute of Ocean Sciences, Fisheries and Oceans Canada, Sidney,
British Columbia, Canada.
differences in responses between the eight experiments. About half of depth-integrated
overall primary productivity is reflected in a decrease of DIC. The overall C/Fe efficiency
of DIC uptake is DIC/Fe 5600 for all eight experiments. The increase of particulate
organic carbon is about a quarter of the primary production, suggesting food web losses
for the other three quarters. Replenishment of DIC by air/sea exchange tends to be a minor
few percent of primary CO
fixation but will continue well after observations have
stopped. Export of carbon into deeper waters is difficult to assess and is until now firmly
proven and quite modest in only two experiments.
Citation: de Baar, H. J. W., et al. (2005), Synthesis of iron fertilization experiments: From the Iron Age in the Age of
Enlightenment, J. Geophys. Res.,110 , C09S16, doi:10.1029/2004JC002601.
1. Introduction
[2] In August 1987, Martin and Fitzwater [1988] demon-
strated that phytoplankton Chl agrowth was strongly stim-
ulated when iron (Fe) was added to bottle-incubated seawater
samples from the subarctic North Pacific (Figure 1a). They
further suggested that Fe limited phytoplankton growth in the
Southern Ocean, another region characterized by chronically
high nutrients and low chlorophyll (HNLC). This long-
forgotten hypothesis of Fe limitation of the Southern Ocean
[Gran, 1931] was tested successfully [de Baar et al., 1990]
1 year later (Figure 1b), with iron addition significantly
stimulating larger diatoms such as Nitzschia fragilaria (sub-
sequently renamed Fragilariopsis kerguelensis),Corethron
sp. and Thalassiothrix sp. [Buma et al., 1991]. With these
events, the iron age in oceanography had begun [Coale et al.,
1999; de Baar and La Roche, 2003].
[3] Nevertheless in both regions the control experiments
also had outgrown the field biomass (Figure 1), hence other
factors such as light limitation and grazing were also at play.
Another major change resulting just from the incubation, was
the marked development of microzooplankton, presumably
due to exclusion of macrozooplankton predators from the
bottles [Buma et al., 1991]. In austral spring 1992, natural
Fe fertilization in the Polar Frontal jet [de Baar et al., 1995]
was found to cause an ecosystem shift-up [Lancelot et al.,
1993, 2000] with the production of vast blooms of large
diatoms, notably Fragilariopsis kerguelensis and Corethron
sp. [Que´guiner et al., 1997; van Leeuwe et al., 1997;
Scharek et al., 1997] and concomitant CO
[Bakker et al., 1997]. Meanwhile, experimental mesoscale
Fe fertilizations of whole ecosystems were proposed as a
direct test of the Fe limitation hypothesis [e.g., Martin,
1992]. The developed sulfurhexafluoride technique (SF
[Upstill-Goddard et al., 1991; Ledwell et al., 1993, 1998;
Law et al., 1994, 1998]) made it possible to mark and track
a patch of water for days to weeks [Martin et al., 1994].
The first in situ Fe fertilization experiment IronEx-1 in
1993 [Martin et al., 1994; Coale et al., 1998] has led to a
suite of now nine such experiments (Table 1) in HNLC
waters (Figure 2).
[4] Among the wide variety of objectives and observa-
tions from these experiments, here only the most striking
aspects of the phytoplankton responses, and the impact on
carbon dioxide (CO
) and major nutrients are presented as
a modest first step to more elaborate synthesis, integration
and generic ecosystem simulation modeling [Hannon et al.,
2001; Pasquer et al., 2005]. Other significant findings have
been or will be reported elsewhere. The responses of
nanoplankton, such as the haptophytes and associated
DMS(P) metabolism, as well the production of several
other biogenic trace gases, have been very well described
[Levasseur, 2002; Turner et al., 1996, 2004; Chuck et al.,
2002; Chuck, 2004; Law and Ling, 2001; Wingenter et al.,
2004; Y. Le Clainche et al., Simulation of the ocean DMS
pool during SERIES: An inverse modeling approach,
submitted to Journal of Geophysical Research, 2005].
Several articles also consider Fe-influenced shifts in Red-
field stoichiometry (C/N/P/Si) [e.g., de Baar et al., 1997;
Takeda, 1998; Frew et al., 2001; Bozec et al.,2005;
Timmermans et al., 2004; Twining et al., 2004a; Marchettti
and Harrison, 2004; Hiscock and Millero, 2005].
2. Iron Fertilization Experiments in the
1993–2004 Era
[5] In October 1993, some 450 kg Fe (7800 mol) together
with SF
tracer (0.35 mol) was introduced into about 64 km
surface waters for the IronEx-1 experiment [Martin et al.,
1994]. A significant increase of photosynthetic quantum
efficiency, Fv/Fm, from 0.3 to 0.6 occurred within 24 hours
[Kolber et al., 1994]. An increase in primary productivity
from 10–15 mg C m
to 48 mg C m
increase of Chl afrom about 0.24 to 0.65 mg m
, and a
modest decrease of fugacity of carbon dioxide, fCO
about 7 10
atm [Watson et al., 1994] were also observed
within the first 3 days. No systematic differences were
observed for the major nutrients (nitrate, phosphate and
silicate) of the fertilized patch compared to out-patch
ambient waters. Unfortunately, the patch subducted to about
30–35 m, after 4 days, and not much happened during the
remaining 5 days of observations [Watson et al., 1994],
apart from some increasing trend of Chl aand a decline in
Fv/Fm [Kolber et al., 1994]. Obviously, the lower light level
at depths exceeding 35 m, was detrimental for further
ecological and biogeochemical response, but the dissolved
Fe within the patch had also decreased below the shipboard
detection limit of about 0.3 nM within 5 days, consistent
with the decrease in Fv/Fm. Afterward, by Fe analyses in
the home laboratory, the final dissolved Fe within the patch
was still above the very low (<0.05 nM) natural dissolved
Fe in ambient waters [Gordon et al., 1998].
[6] The follow-up experiment IronEx-2 in May 1995 was
a major success, and it still is in the context of the seven
subsequent Fe addition experiments (Table 1). One initial
Fe infusion (225 kg) together with SF
tracer at day 0
(29 May), was followed by two more Fe infusions of 112 kg
each at days 3 and 7 [Coale et al., 1996]. The wind mixed
layer (WML) deepened in a suite of small mixing events
from 25 m at day 0 to 50 m by day 11. The Fv/Fm increased
rapidly from 0.25 to 0.5 [Behrenfeld et al.,1996].The
maximum Chl aincreased 27-fold from 0.15–0.20 mg
to values approaching 4 mg m
on day 9, and then
decreased to 0.3 mg m
by day 17. This was accompanied
by a strong nitrate drawdown of 4 mmol m
and a
maximum decrease of fCO
of more than 70 10
atm, also
at day 9 [Cooper et al., 1996, Table 1]. These dramatic
impacts are convincingly illustrated by a day 5 transect
across the patch (Figure 3). A strong initial increase of both
DMSP and its conversion product DMS in the first 6 days
[Turner et al., 1996], followed by a decreasing trend, appears
consistent with a similar increase and then decrease in the
haptophytes, the nanoplankton-sized major producers of
DMSP. All size classes of phytoplankton responded to the
added Fe by increasing their cellular photopigment concen-
tration, indicating that they had previously been Fe limited
[Cavender-Bares et al., 1999]. However the smaller pico-
and nanoplankton size classes were kept at relatively
constant concentrations by heterotrophic grazers, allowing
the initially rare and large (>20 mm) pennate diatom
Pseudo-nitzschia (rather than Nitzschia sp. as reported) to
strongly dominate carbon biomass by the end of the exper-
iment [Cavender-Bares et al., 1999; Landry et al., 2000a,
2000b]. The recently discovered strong organic complexa-
tion of dissolved Fe [Gledhill and van den Berg, 1994; van
den Berg, 1995] was also nicely confirmed with two organic
ligand classes L
and L
in the ambient waters, and a striking
400% increase of Fe(III)-binding ligands, largely in the
stronger L
ligand class, was observed within 48 hours of
Patch-1 Fe fertilization [Rue and Bruland, 1997]. The
Th deficiency method provided a first assessment of
particulate organic carbon (POC) export increasing from
7 mmol m
prior to enrichment to 15 mmol m
in the day 2–7 period, and values approaching 50 mmol
during days 8–14 [Bidigare et al., 1999].
Figure 1. Evidence of Fe-stimulated phytoplankton growth shown as increasing Chl a(mg m
), but
the controls also increase, indicating that other factors (light, grazing) are also important. (left) Deck
incubations of second experiment starting on 6 August 1987, with seawater collected at Station Papa
(50N, 145W) by Martin and Fitzwater [1988], consistent with results of simultaneous experiments of
Coale [1991]. (right) Incubations starting on 8 December 1988, under a controlled light cycle, of seawater
collected in the Southern Ocean (59S, 49W[de Baar et al., 1990]). See original articles and de Baar
[1994] and de Baar and Boyd [2000] for more such experiments.
Table 1. Number, Name, Region, Position, Month(s) by Number, and Year of the Nine In Situ Fe Enrichment Experiments in High-
Nutrient and Low-Chlorophyll (HNLC) Waters in the 1993– 2004 Era
No. Acronym Region Latitude, deg Longitude, deg Month(s) Year
1 IronEx-1 east equatorial Pacific Ocean 05 090 10, 11 1993
2 IronEx-2 east equatorial Pacific Ocean 04 to 07 105 to 111 5, 6 1995
3 SOIREE Southern Ocean (Australian sector) 61 140 2 1999
4 CARUSO/EisenEx Southern Ocean (Atlantic sector) 48 021 11,12 2000
5 SEEDS northwest Pacific Ocean 49 165 7 2001
6 SOFeX-North Southern Ocean (Pacific sector) 56 172 1, 2 2002
7 SOFeX-South Southern Ocean (Pacific sector) 66 172 1, 2 2002
8 SERIES northeast Pacific Ocean 50 145 7 2002
9 EIFEX Southern Ocean 50 002 2, 3 2004
a GreenSea 1 Gulf of Mexico 1 1998
b GreenSea 2 Gulf of Mexico 5 1998
The first and last experiments are briefly or are not discussed here due to early subduction (1) or results still being preliminary (9). Two other experiments
(aand b(for athree patches of 9 mile
, each with chelated Fe, P/Fe = 6.35 and P/Fe = 63.5 additions, for bone patch of 9 mile
with chelated Fe-containing
pellets [Markels and Barber, 2001])) were not in HNLC waters and are not further discussed here either. See original articles for exact daily positions of
drifting patches. Sources are as follows: (1) Martin et al. [1994]; (2) Coale et al. [1996, 1998] (for exact latitude/longitude, see Rue and Bruland [1997];
here only patch 1 of patches 1 –3 is discussed; for test site off California, see Coale et al. [1998]); (3) Boyd et al. [2000] and Law et al. [2001]; (4) Gervais et
al. [2002]; (5) Tsuda et al. [2003]; (6) Coale et al. [2004]; (7) Coale et al. [2004]; (8) Boyd et al. [2004a]; (9) Hoffmann et al. [2005]; (a,b)Markels and
Barber [2001]. The recently published 14 articles with many findings of SEEDS [Tsuda, 2005] have not been incorporated in this synthesis article.
[7] The first Southern Ocean Iron Release Experiment
(SOIREE) [Boyd et al., 2000] took place at the end of
austral summer in February 1999 with four Fe infusions
(days 0, 3, 5 and 7) in the Antarctic Ocean proper, i.e., south
of the Polar Front where all 3 major nutrients silicate, nitrate
and phosphate are present. The depth of the Wind Mixed
Layer was on average about 65 m [Boyd and Law, 2001].
Dissolved silicate at the onset was about 10 mmol m
which is well below winter values. This and the significant
abundance of larger diatoms Fragilariopsis kerguelensis
(>35 mm per cell, 4500 cells L
), and other diatoms
(1900 cells L
) indicated that diatom blooms during
the preceding summer had provided an ‘‘inoculate’’ popu-
lation [Gall et al., 2001a]. Two haptophyte groups, with
pigment signatures typical of Phaeocystis sp. and coccoli-
thophores, respectively, increased steadily during the first
8–10 days, and then decreased somewhat [Gall et al.,
2001a]. This trend was closely correlated with increases
of DMSP and its breakdown product DMS at about
days 89, consistent with cell lysis or grazing, and indeed,
the abundance of heterotrophic ciliates grazers increased as
well on day 9 [Hall and Safi, 2001].
[8] On day 13, the in-patch was dominated by diatoms
[Gall et al., 2001a, Table 2], notably the chain-forming
pennate, Fragilariopsis kerguelensis (16,500 cells L
which has a heavily silicified architecture as grazing pro-
tection [Hamm et al., 2003], and also Rhizosolenia sp.
(4800 cells L
) and Pseudo-nitzschia sp. (1400 cells L
The increasing chain length of Fragilariopsis kerguelensis
(up to 14 cells/chain) indicated favorable growth conditions
(chains up to 40 cells/chain were found in sediment traps
[Waite and Nodder, 2001]). On the final day 13, primary
production was indeed dominated by the >22 mm size class
[Gall et al., 2001b] consisting of diatoms. Among these,
various very large diatom species were abundant, notably
Thalassiothrix antarctica (0.2 cells L
), Asteromphalus
flabellatus (300 mm; 1 cell L
), Trichotoxon reinboldii
(‘‘needles’’ > 1 mm length, and 2 cells L
), Nitzschia
cf. sicula varieties (30 cells L
), Coscinodiscus spp.
(12 cells L
), Eucampia antarctica (0.8 cells L
and various Navicula spp. (3.4 cells L
) as shown by
Waite and Nodder [2001, Figure 1]. These very large
diatoms contribute significantly to the overall diatom bio-
[9] Dissolved nitrate and silicate both decreased by
3 mmol m
during 13 days [Frew et al., 2001]. Similarly
the fCO
and DIC in the patch center had decreased by
about 35 10
atm (Figure 4) and 17 mmol m
, respec-
tively [Bakker et al., 2001]. The area of the fertilized patch
increased from 50 to about 250 km
by day 13, a fivefold
patch dilution constituting a ‘‘chemostat effect’’ where
major nutrients are replenished while the trace element Fe
and plankton biomass are diluted [Abraham et al., 2000].
The observation of the chlorophyll patch by remote sensing
even 40 days after the start of the experiment, also requires
to invoke continuation of a chemostat effect [Abraham et
Figure 2. Chart showing the locations (filled circles) of the nine in situ Fe enrichment experiments
conducted thus far. Moreover, also indicated are the open circle off California for the IronEx test site
[Coale et al., 1998], two open circles for two extra patches during IronEx-2 not further discussed here,
and two experiments GreenSea 1 and 2 at unknown positions in the Gulf of Mexico [Markels and Barber,
Figure 3. Response to Fe enrichment shown by high
fluorescence signal (V) of Chl abeing mirrored by strong
decreases of fugacity of CO
atm)) and
dissolved nitrate (mmol m
) in surface waters of a transect
across the patch during IronEx-2 [Coale et al., 1996;
Cooper et al., 1996] (redrawn after Steinberg et al. [1998]).
al., 2000] and has implications also for self-shading, coag-
ulation and other processes [Boyd and Law, 2001]; yet due to
lack of data in the 13–40 day period these cannot be verified.
For example somehow retention of Fe during 40 days would
presumably be required, somewhat in contrast to some
70% of added Fe being unaccounted for, i.e., lost, within
first 13 days of observations [Bowie et al., 2001].
U ratio was less than 1 before the
experiment, hinting at significant export in the preceding
late summer. During the experiment the
U ratio
increased similarly at both IN and OUT stations by natural
ingrowth of
Th during conditions of near zero net particle
flux [Charette and Buesseler, 2000], consistent with lack of
clear IN versus OUT differences in shallow sediment trap
fluxes [Nodder and Waite, 2001; Nodder et al., 2001].
[11] Comparison of the significant responses between
IronEx-2 in the tropical Pacific and SOIREE in the Southern
Ocean (Figure 5) shows much faster rates of primary
production and nitrate removal in IronEx-2 experiment,
consistent with the far lower temperature, deeper Wind
Mixed Layer (WML) and stronger lateral patch dilution
for SOIREE. This lateral patch dilution may also have
slowed down the aggregation of particles as a step toward
export of larger aggregates in SOIREE relative to IronEx-2
[Boyd et al., 2002].
[12] The Carbondioxide Uptake Southern Ocean
(CARUSO)/Eisen(=Iron) Experiment (EisenEx) took place
in the austral spring, November 2000, in the core of a cold
Antarctic eddy that had spun off the Polar Frontal jet into
the sub-Antarctic region. The eddy being Antarctic water
had all major nutrients present but was surrounded by sub-
Antarctic waters with ample nitrate and phosphate as well,
but low in silicate. Three Fe infusions of 780 kg each at
days 0, 7–8, and 16 were diluted downward and laterally
Figure 4. Significant decrease of fugacity of CO
atm) during the 12 day evolution of the
Southern Ocean Iron Release Experiment (SOIREE) in the Southern Ocean (61S, 140W[Bakker et al.,
Figure 5. Comparison of IronEx-2 and SOIREE. The faster response in (left) primary production and
(right) nitrate removal during IronEx-2 in the equatorial Pacific Ocean is consistent with the lower
ambient temperature, lower PAR, deeper wind mixed layer (WML) depth, and severe lateral patch
dilution during SOIREE.
by two major storms (days 5 and 13) and overall strong
winds throughout the 23 days of observations [Bakker et
al., 2005]. The WML increased from an initial 40 50 m
to almost 100 m during the final days 16 22 (Figure 6).
Patch size increased concomitantly. Shear stress in the
energetic ocean frontal region also played a role in
increasing the patch size from 50 km
during the first
infusion to 950 km
in the final survey map. The
Fv/Fm responded with a slight but distinct increase within
a day [Gervais et al., 2002]. Within 48 hours, Fv/Fm
increased from 0.3 to 0.4 and steadily increased to 0.52 by
final day 21. An increase in primary production on day 2
preceded increases in Chl aon day 4 for all pico-, nano-,
and microphytoplankton size classes (pico < 2; 2 < nano <
20; micro > 20 mm). After day 2, the picoplankton Chl a
remained constant, likely due to a balance between growth
and grazing, but the nanoplankton Chl asteadily increased,
and the initially smallest pool of microplankton Chl a
(>20 mm) increased exponentially to dominate primary pro-
duction after day 16 [Gervais et al., 2002]. The first study of
diurnal carbohydrate dynamics in an enrichment experiment
showed increases of both daytime production and nocturnal
consumption of polysaccharides in Fe enriched waters, the
polysaccharide production furthermore being light limited
[van Oijen et al., 2005]. During the initial phase, the
microplankton diatoms were dominated by Fragilariopsis
kerguelensis with a mean depth-integrated abundance of
5737 cells L
at T= 0 (day 0) of the experiment. This
species increased to 22,146 cells L
inside and 9,389 cells
outside the patch by day 21. Chain lengths on the
order of 4–30 cells/chain were indicative of favorable
growth, with maximum observed lengths of up to 160 cells/
chain. During the second phase of the experiment the smaller
Pseudo-nitzschia lineola became by far the most abundant,
ultimately accounting for 53% of total diatom cells and
25% of total diatom biomass [Assmy, 2004]. A similar
marked response was observed for the small centric diatom
Chaetoceros debilis. Among all diatom species P. lineola
showed the highest accumulation rate of 0.20 d
, and even
outside the patch was growing at 0.09 d
[Assmy, 2004].
By the end of the experiment the depth-integrated cell
numbers of Pseudo-nitzschia had increased 11-fold within
the patch (18.7 10
cells m
) versus the control station
(1.7 10
cells m
). Very large diatoms (e.g., Rhizosolenia
sp., Thalassiothrix sp., Corethron pennatum) also responded
strongly. Although cell numbers of this very large size class
were much lower, in terms of biomass (both organic and opal)
they may be quite significant. Twenty days after the first Fe
infusion, the maximum changes in the surface waters of the
patch relative to the outside patch measurements [Bozec et
al., 2005] were 15 mmol m
for DIC, 23 10
atm for
, +0.033 units for pH, 1.61 mmol m
for nitrate, and
0.16 mmol m
for phosphate (Figure 7). Despite the
significant increase in larger diatoms within the patch, the
dissolved silicate showed a similar decrease of about 4 mmol
for the in-patch and out-patch stations.
[13] The Subarctic Pacific Iron Experiment for Ecosystem
Dynamics Study (SEEDS) enjoyed favorable summer
weather (July 2001) and a shallow 10 m wind mixed layer
during the single infusion of 350 kg Fe and 0.48 M SF
its 8 10 km patch size [Tsuda et al., 2003]. The Fv/Fm of
the whole community rose from a low initial value of 0.2 to
0.3 on day 4, significantly exceeding the out-patch value.
This coincided with the onset of a strong growth phase of
the >10 mm size class on day 4 due to a very rapid increase
of the chain-forming centric diatom Chaetoceros debilis,
which initially had occurred in low numbers (400 cells
at day 0). This gave rise to a very strong increase in Chl
ain the >10 mm size class which fully dominated the total
Chl apool reaching a record of 19 mg m
at the final day
13 of observations (Figure 8). The smaller diatom Pseudo-
nitzschia turgidula [Hasle, 1993] did have higher initial
abundance (10,000 cells L
) but increased slowly and was
surpassed by C. debilis on day 6 in terms of cell numbers.
Similar to the previous IronEx-2 and SOIREE experiments,
albeit more trivial at SEEDS, there was an increase and
finally a decrease, of the nanoplankton (2–10 mm). On the
final day 13 both nitrate and silicate were virtually depleted
(Figure 8), consistent with a decrease again in Fv/Fm on
days 11 and 13 indicative of nutrient stress (N, Fe or both),
and accompanied by record decreases in fCO
(94 10
atm) and DIC (61 mmol m
)[Tsuda et al., 2003].
[14] The Southern Ocean Fe Experiment (SOFeX), in
January–February 2002 increased the effort compared with
the previous experiments by fertilizing two patches (North
and South) at the same time, each patch being larger
(225 km
) than before, with sophisticated multiship logistics
of R/V Revelle,R/VMelville and icebreaker Polar Star
[Coale et al., 2004].
[15] The SOFeX-North patch with low-silicate (<3 mmol
) high-nitrate (20 mmol m
) sub-Antarctic waters, had
two infusions of 631 kg Fe on days 0 and 5 (10 12 and
16 January) and a third 450 kg infusion on day 30
(10 February). The initial WML was 45 m deep increasing
to 55 m 1 month later [Coale et al., 2004, Table S1]. Owing
to many frontal systems in the region, SOFeX-North expe-
Figure 6. Generally high wind velocities (m s
) and two
storms in the Southern Ocean caused a very deep wind
mixed layer (m) during 21 days of the Carbondioxide
Uptake Southern Ocean (CARUSO)/Eisen(=Iron) Experi-
ment (EisenEx) [Bakker et al., 2005].
rienced more shear stress than CARUSO/EisenEx. It was
streaky immediately after the first infusion, and by day 38
the patch had evolved into a 7-km-wide by at least 340-km-
long filament. The Fv/Fm increased from the initial 0.2
to 0.5 at the end. The SOFeX-North patch was character-
ized by an approximately 20-fold increase in Chl a(up to
2.6 mg m
) and a fourfold increase in phytoplankton
carbon biomass. In the early stages (first 2 weeks), the
increase was almost entirely due to >5 mm nonsiliceous taxa
(prymnesiophytes, pelagophytes, dinoflagellates). After a
month, however, >20 mm diatoms, strongly dominated by
Pseudo-nitzschia, had risen from 5 to 38% of total phyto-
plankton biomass despite low available silicate [Coale et
al., 2004; S. Brown and M. Landry, personal communica-
tion, 2005]. Physical mixing and dilution processes
entrained dissolved silicate into the patch [Coale et al.,
2004; Hiscock and Millero, 2005], akin to the chemostat
effect in SOIREE [Abraham et al., 2000]. This prevented
the complete removal of silicate, thus allowing for sus-
tained, however Si-limited, diatom production [Brzezinski
et al., 2005; Hiscock and Millero, 2005]. The maximum
changes in carbonate and nutrient parameters for the North
Patch were 14 ± 5 mmol m
for DIC, 26 ± 5 10
for fCO
,0.09 ± 0.03 mmol m
for phosphate, 1.1 ±
0.4 mmol m
for silicate, and 1.4 ± 0.2 mmol m
nitrate [Hiscock and Millero, 2005].
[16] The SOFeX-South patch in high silicate (60 mmol
) and high nitrate (28 mmol m
) Antarctic waters
had four infusions of 315 kg Fe on days 0, 4, 7 and 11
(24 January–5 February), with the depth of the WML
remaining constant at 35 m [Coale et al., 2004, Table S2].
The study site was strongly dominated by diatoms (2/3 of
phytoplankton C at initial and out-patch ‘‘control’’ stations),
notably Pseudo-nitzschia,Chaetoceros,Thalassiothrix and
Fragilariopsis species and various smaller pennates. The
community-wide Fv/Fm increased from 0.25 to 0.65, and
overall maximum photosynthetic rates increased from 0.29
to 4.6 mmol C m
(Figure 9). Total fluorometric
Chl aincreased by about eightfold, from 0.5 on day 0
to 4 mg m
on day 21. This response comprises a greater
than threefold increase in the phytoplankton Chl a:C ratio,
and slightly greater than a twofold increase in carbon
biomass (M. Landry and S. Brown, personal communication,
2005). Cells in the size ranges of 10–20 and 20 100 mm
showed the highest net rates of change, increasing to about
3 times initial levels, with net rates of change dropping
appreciably for >100 mm cells (very large diatoms) and
negligible change for <10 mm cells. Thus while the commu-
nity response was not dramatic, there was a significant shift
to intermediate and large-sized cells and more diatoms
(increasing from 66 to 80% of phytoplankton carbon bio-
mass) (M. Landry and S. Brown, personal communication,
Figure 8. After a single Fe addition, a record increase in
Chl a(mg m
) and virtual depletion of nitrate (mmol m
and silicate (mmol m
) due to blooming of fast growing
diatom Chaetoceros debilis under favorable WML depth
conditions of the Subarctic Pacific Iron Experiment for
Ecosystem Dynamics Study (SEEDS) experiment in the
northwest Pacific Ocean [Tsuda et al., 2003].
Figure 7. Changes in (a) dissolved inorganic carbon (DIC
(mmol kg
mol kg
seawater)), (b) fugacity of
atm), and (c) nitrate + nitrite (mM = mmol m
during 21 days of the CARUSO/EisenEx experiment in the
Southern Ocean [Bozec et al., 2005]. Dotted lines indicate
heavy storm events at days 5, 13, and 17.
2005). The maximum changes of carbonate parameters in
the South Patch mixed layer were 21 ± 5 mmol m
DIC and 36 ± 4 10
atm for fCO
[Hiscock and Millero,
2005]. The maximum changes for nutrients were 0.22 ±
0.03 mmol m
for phosphate, 3.6 ± 0.2 mmol m
silicate, and 4.1 ± 0.2 mmol m
for nitrate [Hiscock and
Millero, 2005]. Changes in the carbonate and nutrient
systems of the South Patch were larger than those in the
North Patch. In addition, the export of carbon as particles
settling into deeper layers was determined to be significant
by the
Th deficiency technique (Figure 9), but modest
with respect to regular estimates in the region [Buesseler et
al., 2004, 2005].
[17] During summer of the same year (July 2002), another
multiship experiment, the Subarctic Ecosystem Response to
Iron Enrichment Study (SERIES) was conducted at ocean
station ‘‘Papa’’ (50N, 145W) where it all had started
[Martin and Fitzwater, 1988]. Upon two Fe infusions (days
0 and 6) of the quite favorable fairly shallow 30 m WML
depth, the 77 km
patch enlarged to >200 km
by day 13
and to a maximum of about 1000 km
by days 17–18 [Boyd
et al., 2004a]. The Fv/Fm increased from an initial value of
0.2 to at most 0.4 by day 11, dropping to about 0.2 by day
19 then decreasing further to well below 0.2 at day 21 [Boyd
et al., 2004a, suppl. Figure 1]. The Chl aincreased
[Harrison et al., 2004] from an initial 0.6 mg m
to a
maximum 5.5 mg m
on day 17, then dropped sharply to
about 1.5 mg m
by days 23–25 (Figure 10). The parallel
increase of diatom biovolume was stronger relative to the
low initial values, and the strongest increase (days 10 15)
was nicely mirrored by a sharp decrease in dissolved silicate
(Figure 10). The most dramatic blooming was by the small
pennate diatom, Pseudo-nitzschia sp., which increased from
an initial 174 cells L
to 192,000 cells L
at peak days
15–18 [Marchettti and Harrison, 2004]. Similarly the
almost 100-fold larger cells of the pennate Thalassiothrix
increased from 17 to 12,100 cells L
, thus dominating by
some 33% the carbon inventory of all diatoms. Centric
diatoms of medium (Chaetoceros sp.), large (Thalassiosira,
Proboscia) and very large (Rhizosolenia) sizes, together
comprised over 60% of the diatom carbon inventory. On
about day 16, silicate was depleted, and the bloom declined,
leading to increased export flux into sediment traps at 50,
75, 100 and 125 m (Figure 10). This, and the above-
mentioned export flux at SOFeX-South, were the first
convincing observations of Fe-stimulated export of POC
and Si into deeper waters. Over the 25 day experiment,
about 14 mmol m
silicate and 5 mmol m
nitrate were
removed (Figure 10). The fCO
showed its maximum
decrease of over 70 10
atm in the patch centre at day
Figure 9. (top) Upon four consecutive Fe fertilizations (arrows on top) of the large 255 km
South patch
of Southern Ocean Fe Experiment (SOFeX), dramatic increase (filled dots) of the primary production
(mmol C m
) compared to the out-patch development (open circles) [Coale et al., 2004]. For exact
times of fertilizations, see Coale et al. [2004, Tables S1 and S2]. (bottom) Significant increase of the
particulate organic carbon (POC) export (mmol C m
) across the (a) 50 m and (b) 100 m depth
horizons at the end of day 28 of the SOFeX-South patch (in iron, filled) and control site (out of iron,
shaded), derived from the
Th deficiency method (redrafted after Buesseler et al. [2004]).
18 [Boyd et al., 2004a, supplement]. On the same day, DIC
had decreased by about 40 mmol m
, but then it increased
again due to the combined effects of bloom decline (respi-
ration) and patch dilution with ambient waters.
[18] Finally the very recent EIFEX experiment (2004) in
the Southern Ocean is mentioned but results are not yet
3. Light Limitation and Other Physical Forcings
[19] Wind mixing strongly influences the amount of light
that phytoplankton receive for growth. When comparing the
eight Fe experiments there is a wide range of average depths
of the wind mixed layer (Figure 11, black bars), which vary
from a shallow 10–15 m for SEEDS to 100 m for
CARUSO/EisenEx (Figure 6). The maximum yield of Chl
aabundance shows an inverse relationship with WML
(Figure 11, green bars).
[20] Excluding IronEx-1, which is anomalous due to early
subduction, one finds a striking and significant (R
= 0.90)
inverse relationship between maximum Chl ayield and
average WML depth (Figure 12 (top)). Hence having
dumped a total of 8795 kg of Fe into HNLC waters and
utilizing about 1 year of shiptime, we may conclude that
Figure 10. Subarctic Ecosystem Response to Iron Enrich-
ment Study (SERIES) experiment in the northeast Pacific
Ocean: (top) the initial strong bloom development of (red)
Chl a(mg m
) and (blue) diatom biovolume (mL m
seawater) eventually led to (middle) nutrient depletion,
causing a decline of the bloom after day 18 (upper panel) as
well as a significant increase in settling particles exported
into (bottom) deeper waters. Solid symbols are in patch,
open symbols are out of patch (graphics after Boyd et al.
Figure 11. Comparison of WML depth and maximum
observed abundance (Chl a) or concentration change in the
patch for eight experiments; some variables are scaled such
that all fit a common 0 100 vertical axis. WML depths are
as reported for each experiment; see source articles for
WML definition criteria (e.g., density gradient) of any given
experiment. For SOFeX the WML values are after Coale et
al. [2004, Tables S1 and S2], rather than deviating values in
the printed article. Black is WML depth (m), green is
fivefold the maximum observed Chl a(mg m
), dark blue
is 10-fold maximum observed nitrate removal (mmol m
light blue is threefold maximum observed silicate removal
(mmol m
), yellow is maximum observed decrease in
fugacity of CO
atm), and red is maximum observed
DIC removal (mmol m
). Sources are as follows: Cooper
et al. [1996]; Bozec et al. [2005]; Bakker et al. [2005];
Hiscock et al. [2002]; Hiscock and Millero [2005]; Tsuda et
al. [2003]; Coale et al. [2004]; and Boyd et al. [2004a].
light is the ultimate determinate of the phytoplankton
biomass response. However, Chl amay not be the most
suitable variable for biomass. Since iron is required for
synthesis of the chlorophyll molecule, and Fe-depleted
phytoplankton tend to be short in Chl a, one of the first
responses to Fe enrichment is an increase in cellular Chl a
(Figure 13). For example, the mean C:Chl ratio of phyto-
plankton decreased by factors of 4 5 in the IronEx-2 and
CARUSO/EisenEx patches [Landry et al., 2000a; M. J. W.
Veldhuis and K. R. Timmermans, Photoplankton dynamics
during the EISENEX in situ iron fertilization experiment
in the Southern Ocean: A comparative study of field and
bottle incubation measurements, submitted to Limnology
and Oceanography, 2005] and only slightly less in
SOFeX-South (M. Landry, personal communication,
2005). Since Chl ayield exaggerates the phytoplankton
biomass response to Fe fertilization, a more suitable
indicator may be preferable.
[21] Both the maximum nitrate removal and the maxi-
mum fCO
drawdown (Figure 11, blue and red bars,
respectively) also show trends opposite to the WML depth,
but the fits (R
= 0.69 and R
= 0.63, respectively) are less
convincing (Table 2). Perhaps the maximum net removal
(photosynthesis/respiration) of DIC, which also shows an
inverse trend with WML depth (Figure 11) with a better fit
= 0.72; see Figure 12 (bottom)), is the most suitable
overall biomass indicator.
[22] Of course other physical factors are also at play here.
First, the amount of incident light at the sea surface, or
photosynthetically active radiation (PAR), varies from day
to day, by region and by season (Figure 14). Moreover,
when a bloom develops, the self-shading by the more
abundant phytoplankton diminishes the available light be-
low, and thus the maximum extent of the euphotic zone of
positive phytoplankton growth (not shown).
[23] The optimal or maximum rate of growth (m
Monod [1942]) is well known to be a function of tempera-
ture, where for each 10C rise in temperature the maximum
growth rate doubles [Eppley, 1972; Goldman and Carpenter,
1974]. Given the range in temperatures (Figure 14) one
would expect the primary production during IronEx-2
(25C) to be almost fourfold faster than during SOIREE
(2C), and such trend is apparent indeed (Figure 5).
[24] Similarly, SEEDS (9.5C) showed growth rates
about 50% faster than CARUSO/EisenEx. In fact, during
days 4–7 of SEEDS, the major diatom C. debilis grew at a
net rate of 2.6 doublings/day (m= 1.8 d
), exceeding the
expected maximum of 1.5 doublings/day (m= 1.0 d
9.5C[Tsuda et al., 2003].
Figure 12. (top) Apparent inverse and significant relation-
ship between the maximum observed Chl aabundance
(mg m
) and WML depth (m) for seven experiments. The
probability that the fitted curve with an exponent of 1.342
is due to chance alone is low enough (P= 0.003, t=5.55,
= 0.90, n= 7) to reject the hypothesis that WML depth
has no effect. Excluded is IronEx-1 for its somewhat
anomalous premature end on day 4 due to the subduction of
the patch. (bottom) Same for maximum observed removal
of DIC (mmol m
Figure 13. Amount of Chl aper cell (femtogram cell
increased about fourfold in the most stimulated largest
size class (>8 mm) eukaryote phytoplankton (i.e., diatoms)
during the first 19 days of the CARUSO/EisenEx
experiment (data of M. J. W. Veldhuis). Such an increase
of cellular Chl awas evident already from the C/Chl a
ratio in one of the first bottle experiments [Coale, 1991,
Figure 6] and in IronEx-2 [Cavender-Bares et al., 1999].
In retrospect, this also indicates that Chl aexaggerates the
phytoplankton biomass response to added Fe (Figures 11
and 12).
10 of 24
[25] Finally, due to combined wind mixing and shear
stress, the initial patch tends to dilute, somewhat by mixing
with underlying waters, but apparently more by lateral
mixing. With most initial patch size areas of about 50
80 km
, and 225 km
for SOFeX patches, the final patch
area after 13 38 days of observations may well exceed
2000 km
(Figure 15). Obviously the resulting dilution
factor will be least at the patch centre and increase toward
its edges, and in principle can be assessed from the distri-
bution of SF
tracer in time and space, after a correction for
loss by gas exchange. However, matters are complicated
by the need for several Fe infusions, while only the first
infusion included the SF
tracer. Also, patches can evolve
very chaotically (CARUSO/EisenEx, SOFeX-North) defy-
ing quantitative description. Here, we simply have taken the
ratio of initial patch size and reported final patch size as
indicative of lateral patch dilution. This dilution factor varies
from 3 and to 19, where obviously the length in days of the
experiment plays a role (Figure 15 and its caption).
4. Linking the Peaceful Pacific With the
Roaring Forties
[26] Given the wide range in physical conditions (WML
depth, PAR, temperature, patch dilution) and biogeochem-
ical responses (Figures 11, 14, and 15), we will take up the
challenge of determining coherence between only the two
extreme cases: SEEDS with favorable conditions and record
responses, and CARUSO/EisenEx.
[27] After completing the 15 hours of the first Fe infusion
for CARUSO/EisenEx, seawater samples were immediately
collected in both the in-patch and at an out-patch control
station. This seawater was placed in a suite of PMMA
bottles (transparent for UVB + UVA + visible light) in deck
incubators with screening to simulate a 12 ± 4 m light depth
[van Oijen and Rijkenberg, 2004], as well as in large 20 L
polycarbonate bottles incubated under artificial light on a
12/12 hour day/night cycle at a light level (3.5 mol m
corresponding to the 25 m light depth (K. R. Timmermans
et al., manuscript in preparation, 2005). The PAR reach-
ing the sea surface as well as the screened deck incuba-
tors varied between 12 and 55 mol m
, averaging
30 mol m
[28] Four cases can now be compared. The CARUSO/
EisenEx in situ in-patch stations reached a maximum nitrate
removal of 1.6 mol m
after 21 days (Figure 7 (bottom)).
The in-patch samples of the CARUSO/EisenEx deck incu-
bators were completely depleted of both nitrate and silicate
after 12–14 days (Figure 16 (left)), strikingly similar to the
SEEDS in situ result after 13 days (Figure 8). In these deck
incubators, the same diatoms as found in the field showed
healthy net growth rates of 0.40.6 d
, with significantly
(10–15%) higher growth for the Fe-fertilized in-patch
bottles, notably for Pseudo-nitzschia which eventually was
dominant both in these bottles and in the in situ in-patch
stations [van Oijen and Rijkenberg, 2004].
[29] Remarkably, only Fragilariopsis kerguelensis did
not show higher growth rates for the Fe-enriched in-patch
bottles versus control out-patch bottles. This is consistent
with its failure to eventually dominate the in situ in-patch
stations (as opposed to SOIREE). Finally, the CARUSO/
EisenEx in-patch samples cultured under lower artificial
light were somewhat slower, only exhausting nitrate and
silicate after 18 days (Figure 16 (right)).
[30] When comparing the physical forcing parameters
temperature, WML depth and the patch dilution factor for
Table 2. Apparent Inverse Relationships of Wind Mixed Layer (WML) Depth Versus Observed Maximum Chl
aand Versus Observed Maximum Removals of Nitrate, Fugacity of CO
, and Dissolved Inorganic Carbon (DIC)
in Seven Experiments
Function of WML Depth Best Fit R
Maximum chlorophyl = f(WML) y= 523.21 x
(exponential) 0.90 7
Maximum delta nitrate = f(WML) y= 82.33 x
(exponential) 0.69 7
Maximum delta fCO
=f(WML) y=1.087 x+ 97.62 (linear) 0.63 7
Maximum delta DIC = f(WML) y=0.772 x+ 59.04 (linear) 0.72 7
WML depth is in meters. Observed maximum Chl ais in mg m
. Fugacity of CO
is in 10
atm. Dissolved inorganic
carbon is in mmol m
. The probability that the fitted curve of Chl aversus WML with an exponent of 1.342 is due to chance
alone is low enough (P= 0.003, t=5.55, R
= 0.90, n= 7) to reject the hypothesis that WML depth has no effect. Excluded is
IronEx-1 due to premature end at day 4 by patch subduction. The better fits for Chl aand for DIC are illustrated in Figure 12.
The goodness of fit R
for n= 7 data points is remarkable but certainly not perfect due to several other factors (temperature,
photosynthetically active radiation, patch dilution, grazing, and K
for Fe limitation of predominantly responding
phytoplankton species) also playing roles; see text.
Figure 14. (top) Average temperature (C) in surface
waters. (bottom) Photosynthetic active irradiance (PAR)
(mol m
) at the sea surface; average value over the
given experiment. Day-to-day variability indicated by error
bars (two sigma standard deviation of the daily values for
the given experiment) is small in equatorial IronEx-1 and
IronEx-2 and large in EisenEx.
11 of 24
the two extreme in situ experiments CARUSO/EisenEx and
SEEDS (Figure 17 (top)), one notices that simulated WML
depths of the CARUSO/EisenEx bottle treatments are
similar to, or slightly deeper, than for SEEDS. Moreover,
bottles obviously have a dilution factor of 1 (no dilution),
closer to the modest factor of 3 of SEEDS than the large
dilution factor of 19 for CARUSO/EisenEx. The resulting
daily removal rates of nitrate and silicate (Figure 17
(bottom)) in both bottle treatments nicely bridge the gap
between the nutrient removal rates of the two in situ
experiments. The fact that both nutrients are also fairly
rapidly removed in the control treatments (Figure 16),
further confirms the major impact of light relative to Fe
deficiency. Even though the differences of PAR as well
as temperature between CARUSO/EisenEx and SEEDS
(Figure 14) have been ignored here, the strong influence
of WML depth, defining the mean light environment, as
well as the dilution factor, is very obvious. Admittedly,
this is just a very simple approach, only providing a
working hypotheses for a more refined validation of day-
to-day changes in these four cases by plankton ecosystem
modeling [Lancelot et al., 2000; Pasquer et al., 2005],
with all physical forcings (WML depth, PAR, dilution
factor, temperature) in the model varying daily and acting
5. Large Diatoms
[31] In all of the experiments, added Fe produced a
striking shift-up response of cell numbers of larger size
classes of diatoms. In general the community biomass
shifted from mostly nanoplankton (<10 mm) to mostly
microplankton (>10 mm). As noted previously, the interme-
diate-sized pennate (Pseudo-) Nitzschia sp. took over in
Figure 15. (top) Initial patch area (km
) compared with
(middle) final patch area (km
) (note 10-fold larger vertical
scale) and (bottom) their derived ratio (final/initial) or patch
dilution factor. Patch dilution factor obviously also tends to
increase with the length (days) of the observation period:
IronEx-2 was 17 days, SOIREE was 13 days, EisenEx was
23 days, SEEDS was 13 days, SOFeX-North was 38 days,
SOFeX-South was 20 days, and SERIES was 18 days at
bloom optimum and 23 days overall.
Figure 16. (left) Rapid removal of dissolved nitrate (mmol m
) and silicate (mmol m
) in deck
incubations at 8–16 m simulated light depth of in-patch (filled symbols) and out-patch (open symbols)
of 20 L seawater during CARUSO/EisenEx [van Oijen and Rijkenberg, 2004]. (right) Similar but under
controlled 12 hour light/12 hour dark cycle with 3.5 mol m
light level corresponding to a 25 m
simulated light depth during EisenEx (K. R. Timmermans et al., manuscript in preparation, 2005).
12 of 24
IronEx-2 [Landry et al., 2000a]. Pseudo-nitzschia species
also dominated in CARUSO/EisenEx, SOFeX-North and
SERIES. The large chain-forming pennate Fragilariopsis
kerguelensis was most successful in terms of cell numbers
in SOIREE, consistent with its spring bloom development
and dominance in the naturally Fe-rich Polar Frontal jet [de
Baar et al., 1995, 1997]. Both Fragilariopsis kerguelensis
and Pseudo-nitzschia were numerically dominant in
SOFeX-South, also at the control stations. During SEEDS,
the centric chain-forming Chaetoceros debilis responded
very strongly, replacing the smaller pennate Pseudo-
nitzschia turgidula in both cell abundance and biomass
after 6 days. These in situ results are consistent with the
major conclusion of a preceding synthesis of all preceding
bottle incubation experiments and natural Fe-replete regions
which documented a systematic Fe stimulation of the large
size class of diatoms [de Baar and Boyd, 2000].
[32] Reports on very large diatoms (0.1 1 mm) have
been relatively sporadic. Nevertheless, very large taxa
(Rhizosolenia sp., Thalassiothrix,Thrichotoxon,Asterom-
phalus,Actinocyclus sp.) with elongate ‘‘needles’’ as well as
perfectly discoid forms should not be overlooked. In terms
of biomass (organic matter or opal), these ‘‘giants’’ may in
some experiments have grown to higher levels than the
numerically more abundant (cells m
) large diatoms.
[33]Timmermans et al. [2001a, 2001b, 2004] have suc-
ceeded in maintaining such very fragile (spines, weak
chains) diatoms of moderate (10 30 mm), medium (30–
60 mm) and large (>60 mm) size classes in cultures of natural
(no EDTA disturbances [Gerringa et al., 2000]) Antarctic
seawater. From their curves (not shown) of growth rate
responses versus added dissolved Fe, the constants K
half-saturated growth (= 50% of maximum growth rate)
now show a convincing inverse relationship with surface/
volume ratio (Figure 18). Since surface/volume ratio is itself
inversely related to size, the required ambient Fe concen-
tration to achieve 50% of maximum growth rate clearly
increases as a (fairly linear) function of diatom size.
Moreover, the required Fe concentrations (0.2 1.2 nM)
are above the typical dissolved Fe concentrations of remote
oceanic surface waters. In other words, these size classes
of moderate (10–30 mm), medium (30 60 mm) and large
(>60 mm) diatoms can only bloom upon an extra delivery of
dissolved Fe, either by wet dust deposition from above
[Jickells and Spokes, 2001], by an Fe-rich oceanic front [de
Baar et al., 1995, 1997], by an upwelling/mixing supply
event from below [Hoppema et al., 2003], by iron supply
from shallow topography [Blain et al., 2001], or by an in
situ Fe fertilization experiment.
[34] The observed linear relationship between diatom
size and Fe requirement for growth is a major step forward
and key to understanding the in situ experiments. When
superimposing the above K
of the large F. kerguelensis
and very large Actinocyclus on the time series of dissolved
Fe (<0.2 mm filtrate) in SOIREE, the minimum observed
dissolved Fe is more or less adequate to support half-
Figure 17. (top) Case study linking EisenEx and SEEDS
by comparison of different physical forcings, temperature
(C), WML depth (m), and dilution factor, with (bottom)
resulting daily nutrient removal rates (mmol m
). Not
shown in Figure 17 (top) is the different forcing by incident
light PAR averaging 31.1 mol m
during EisenEx and
29.96 mol m
during SEEDS.
Figure 18. Inverse relationship between surface/volume
ratio of medium-sized and large-sized Antarctic diatoms
versus the half-saturation value K
for growth m/m
+ [Fe]) after Monod [1942]. Shown are large
Fragilariopsis kerguelensis and larger Corethron pennatum,
Thalassiosira, and very large Actinocyclus sp., the latter
very similar in perfect discoid shape and 300 400 mm size
as Asteromphalus sp. [Waite and Nodder, 2001]. Graph
plotted after K
data of dissolved Fe (nM) growth curves
(not shown here) in natural Antarctic seawater; see
Timmermans et al. [2004] for these growth curves.
13 of 24
maximum growth of F. kerguelensis, but inadequate for
Actinocyclus (Figure 19). The double Fe concentrations
(dotted lines) for optimal 100% growth are occasionally
met for F. kerguelensis and rarely, if at all, for Actinocyclus.
Obviously, if one could maintain a steady and carefully
chosen dissolved Fe concentration throughout an experi-
ment, the relationship (Figure 18) might reliably predict the
size class of diatom that would dominate in the end (in the
absence of loss processes to grazing, sinking, etc.).
[35] Even this, however, has proven to be a major
stumbling block of the in situ experiments. The intrinsic
instability of the added reduced Fe(II) in oxygenated sea-
water (discussed below) leads to rapid removal of the Fe
enrichment. In an effort to remedy this problem, a lignopo-
lysulfonate ligand had been added during the two experi-
ments (GreenSea 1, 2) in the Gulf of Mexico (Table 1), but
its effect cannot be discerned from the brief report [Markels
and Barber, 2001]. In all other experiments, only dissolved
[Fe(II)] was added.
[36] In SOIREE, four successive Fe additions (vertical
black bars) were applied in an effort to compensate for the
major Fe loss. Despite a rigorous budgeting approach
[Bowie et al., 2001], only 30% of the added Fe could be
accounted for, the remaining 70% being ‘‘lost.’’ Similar
repeat Fe infusions have been done for most other experi-
ments (except IronEx-1 and SEEDS), with Fe budgeting
hardly, if at all, being attempted anymore. The overall result
tends to be a sawtooth pattern of dissolved Fe concentration
inside the patch.
[37] This sawtooth pattern creates a conceptual dilemma
in which the K
values (Figure 18) are only valid at steady
state, i.e., constant dissolved Fe, while patch in situ Fe
concentrations oscillate markedly. Presumably, during
events of high natural input of dissolved Fe, diatoms are
capable of luxury accumulation of Fe within their cells, to
be used later when Fe concentration fall below a critical
threshold level, e.g., K
. Perhaps for any given diatom
species, a bandwidth of suitable dissolved Fe between, for
example, 50% and 100% of optimal growth, defines the
range to be maintained in an in situ experiment. Future
culture experiments exposing diatoms to oscillating Fe
levels may demonstrate such Fe storage capacity and help
bridge the conceptual gap between our present understand-
ing of linear steady state relationships (Figure 18) and the
more dynamic algorithms that will be needed for the next
generation of ecosystem simulation models of in situ experi-
ments [Lancelot et al., 2000; Hannon et al., 2001]. Obvi-
ously, this is also desirable for understanding the real ocean
where natural dissolved Fe varies over daily timescales in
surface waters.
6. Fe Chemistry in Seawater
[38] Until now, the role of Fe has been described using
dissolved Fe in filtered seawater (<0.2 mm filtrate) as the
common variable. In reality, however, the physical chemis-
try of Fe in seawater is far more complicated.
[39] During CARUSO/EisenEx, polyethylene hollow-
fiber ultrafiltration was used to distinguish another size
class, colloids (200 kDa < colloids < 0.2 mm), with the
ultrafiltrate (<200 kDa) being called the soluble fraction
[Nishioka et al., 2005]. Prior to the first infusion of iron, the
dissolved (<0.2 mm) iron concentrations in the ambient
surface seawater were extremely low (0.06 ± 0.015 nM),
with colloidal iron being a minor fraction. For the iron
addition, the eddy was fertilized with an acidified FeSO
solution (i.e., reduced [Fe(II)]) 3 times over a 23 day period
[de Baar, 2001]. High concentrations of dissolved iron
(2.0 ± 1.1 nM) were measured in the surface water until
4 days after the first iron infusion (Figure 20). After every
iron infusion, when high iron concentrations were observed
before storm events, there was a significant correlation
between colloidal and dissolved iron:
Colloidal Fe½¼0:7627 Dissolved Fe½þ0:0519;R2¼0:93:
These results indicate that a roughly constant proportion of
colloidal versus dissolved iron (76%) was observed after
iron infusion. Thus it appears that most of the added [Fe(II)]
was rapidly converted into fine colloids.
[40] The operationally defined division of Fe into three
size classes, soluble <200 kDa, 200 kDa < colloids < 0.2 mm,
and particles >0.2 mm, is also reflected in the organic
complexation of iron. Organic binding of Fe was investi-
gated only in the soluble and colloid fractions [Boye´etal.,
2005]. In the natural seawater before Fe addition, some 91 ±
3% of the organic Fe-binding ligands was found in the
soluble fraction. In contrast, the size distribution of ligands
in the mixed layer after Fe release was balanced between
soluble (55%) and colloidal (45%) ligands. Soluble
and colloidal ligands were produced rapidly within the
mixed layer after the first and second Fe infusions. Here a
dramatic increase of the colloidal ligand concentrations
was observed, increasing concentrations by two- to three-
fold for soluble, and up to 35-fold for colloidal ligands,
relative to their respective out-patch levels.
Figure 19. K
value of dissolved Fe (nM) for 50% of
optimal growth rate (lines) and optimum 100%, i.e., double
or maximum growth rates (horizontal dotted lines) for
large Fragilariopsis kerguelensis and very large Actinocy-
clus sp. superimposed on the sawtooth pattern of averaged
dissolved Fe observed in the in-patch of SOIREE (filled
triangles) as a result of imbalance of rapid Fe losses and
four consecutive Fe releases. Open triangles connected with
bold dotted line is averaged dissolved Fe at the control (out)
station. Graph drawn after Bowie et al. [2001] and
Timmermans et al. [2004].
14 of 24
[41] Simultaneous measurements of Fe(II) and H
showed detectable Fe(II) concentrations for up to 8 days
after iron infusion [Croot et al., 2005]. Vertical profiles of
Fe(II) showed maxima consistent with the plume of the iron
infusion. Parallel H
profiles revealed corresponding
minima, showing the effect of ongoing oxidation of Fe(II)
by H
. The H
concentrations increased at the depth
of the chlorophyll maximum when iron concentrations
returned to preinfusion concentrations (<80 pM), possibly
due to biological production related to iron reductase
activity. During a later surface survey of the iron enriched
patch, elevated levels of Fe(II) were found in surface
waters presumably from Fe(II) dissolved in the rainwater
that was falling at this time. Model results suggest that
the reaction between uncomplexed Fe(III) and O
was a
significant mechanism helping to maintain high levels of
Fe(II) in the water column, and the low temperature of
Antarctic seawater slows down the reverse oxidation
reaction considerably [Croot et al., 2001]. Finally, pho-
tochemical reduction of finely dispersed colloids may act
as a source of reduced [Fe(II)] in surface waters [Rijkenberg
et al., 2005], thus making Fe available again for plankton
[42] We are only beginning to understand the chemistry
of Fe in seawater. Nevertheless two main lines of thought
can already be identified.
[43] First, the artificial 100-fold increase of overall Fe
levels after the addition of dissolved inorganic Fe(II) ions is
a major disruption of the natural physical-chemical abun-
dances and reactivity of Fe in seawater. Hence the ensuing
plankton responses, while significant, are not necessarily
representative of natural enrichment by dry or wet deposi-
tion of aeolian dust [Boye´etal., 2005], or from adjacent
continental margins or ocean island plateaus. This notion
has led to another experiment (FeCYCLE, 2003) where
only SF
tracer was added just to follow the natural physical
chemistry of Fe in seawater [Boyd et al., 2004b] (available
at Moreover, two parallel
programs BICEP and KEOPS were undertaken in austral
summer 2004–2005 using natural gradients of dissolved Fe
near the ocean islands of Crozet and Kerguelen [Blain et al.,
2001; Bucciarelli et al., 2001] as a natural laboratory for
unraveling the complex interactions of Fe chemistry and
phytoplankton growth.
[44] Second, algal cells can only directly assimilate
‘‘truly dissolved’’ Fe and thus the Fe residing within the
Figure 20. During EisenEx the operationally defined ‘‘dissolved’’ Fe (nM) in seawater (filled dots) in
fact consisted of a constant major 76% portion of fine colloids in the >200 kDa size class (open squares).
Only the remaining 24% soluble Fe (open triangles) is deemed to be directly available for uptake by
phytoplankton [Nishioka et al., 2005]. Photoreduction of some colloids in daytime to Fe(II) (not shown
here; see Croot et al. [2005]) is partly responsible for maintaining the soluble fraction, where organic
complexation in both colloid and soluble fraction also plays a role (not shown here; see Boye´etal.
[2005]). The rapid formation of colloids and then their conversion into larger (>0.2 micron) particles
surely is the major route by which much added Fe is lost, therefore necessitating repeat Fe additions.
Otherwise, some of the colloids may dissolve again by photoreduction [Rijkenberg et al., 2005], and
some particulate Fe may dissolve again by grazing [Barbeau and Moffett, 2000]. More research is needed
to assess how these processes interact and how they may together indirectly supply Fe for uptake by
15 of 24
soluble (<200 kDa) size fraction. This soluble fraction
consists of reduced [Fe(II)] as well as organically bound
[Fe(III)ligand], with evidence for more than one ligand
type, and also some inorganic [Fe(III)]. It is not clear which
is the preferred form for uptake by algae. If the kinetics of
exchange between these three major forms within the
soluble pool are faster than the overall uptake rate, algal
uptake preferences do not really matter. On the other hand,
if one or more of the transformation reactions are slow, it
(they) could potentially control growth rates of the algae.
Moreover, the colloid size class (>200 kDa) is not directly
available for uptake, but may rapidly replenish the soluble
pool, as colloids dissolve by photoreduction [Rijkenberg et
al., 2005], releasing dissolved [Fe(II)] for algal uptake. Yet,
in due course, the [Fe(II)] will also be oxidized again into
colloids. The kinetics of exchange between these various Fe
pools must be quantified in order to understand how Fe
controls the rate of phytoplankton growth. Thus the above
consistency between K
values (Figure 18) from diatom
growth curves [Timmermans et al., 2004] and dissolved Fe
(<0.2 mm fraction) during an in situ experiment (Figure 19)
is an important step forward, but only one step on a long
road to unraveling the complexities of iron-phytoplankton
7. Grazing Impacts
[45] In discussing the potential roles of grazers in Fe-
fertilized ecosystems, it is useful to distinguish between two
major size classes: the micro- and mesozooplankton. Oper-
ationally, the ‘‘microzooplankton’’ includes all consumers
<200 mm in size, a size class typically dominated by a
diverse assemblage of heterotrophic and mixotrophic pro-
tists. Such organisms are the major direct consumers of
phytoplankton in the open oceans [Calbet and Landry,
2004], and can grow at rates comparable to or greater than
similarly sized phytoplankton. Because of these qualities,
meaningful studies of the grazing impacts and population
responses of the microzooplankton can be conducted on the
days-to-weeks scale of the typical fertilization experiment.
The ‘‘mesozooplankton,’’ on the other hand, are larger
(>200 mm) animals with longer and more complex life
histories, some (in polar and subpolar systems) with gener-
ation times of a year or more. Mesozooplankton play central
roles in ocean food webs as consumers of large phytoplank-
ton, as trophic intermediates to higher-level consumers (e.g.,
fish), as fecal pellet producers (thereby accelerating sinking
and export flux), and as predators and regulators of the
microzooplankton, all of which make them relevant to
understanding system level responses to Fe. However, the
temporal and spatial scales of experimental studies con-
ducted to date are inadequate to study population and
community responses of mesozooplankton to Fe, or to
predict their direct and indirect implications for large-scale
and long-term Fe fertilization. Because our current under-
standing of Fe effects on ocean ecosystems does not extend
past single-celled organisms, the comments below are
meant to apply mainly to this ‘‘microbial’’ portion of
plankton communities.
[46] Since Fe concentration strongly affects growth rate
and, therefore, the intrinsic competitiveness of phytoplank-
ton taxa and size classes (Figure 18) and since light-related
variables, like WML depth, appear to control maximum
levels of biomass accumulation (Figure 12), grazing inter-
actions would seem, at first glance, to have little influence
on phytoplankton responses to Fe addition. However, tem-
poral changes in populations and communities do not
simply reflect growth rates or potential, but rather the net
realized differences between growth and mortality rates.
Consequently, if the goal is to predict the timing and
magnitudes of Fe responses at the community and system
levels, the mortality ‘‘environment’’ is as important as the
growth environment for determining net rates of change.
The role of mortality becomes particularly apparent when
one considers how initially rare taxa rise to dominance
quickly in Fe fertilization experiments. In IronEx-2, for
example, the estimated Fe stimulated growth rate for
the diatom Pseudo-nitzschia was 2 cell doublings d
(m= 1.4 d
[Landry et al., 2000b]) while Prochlorococcus
growth rate was observed to shift up from 0.7 d
1.1 d
when Fe was added [Mann and Chisholm, 2000].
If left entirely to the growth rate difference of 0.3 d
initially rare Pseudo-nitzschia would need about 8 days of
growth (16 generations) to catch up to Prochlorococcus for
each order-of-magnitude difference between the two in
their initial contributions to community biomass. In reality,
Pseudo-nitzschia was rapidly installed as the bloom dom-
inant within 5 days of the IronEx-2 patch fertilization
because Prochlorococcus and other small cells were held
entirely in check by grazing (Figure 21). For these initially
dominant phytoplankton, already growing at relatively high
rates under ambient conditions, the adjustments that lead to
continued grazing balance at Fe-stimulated rates of growth
Figure 21. Phytoplankton community size structure in the
ambient environment (CONTROL) and the iron-fertilized
PATCH during IronEx-2 (May–June 1995). Carbon
estimates are based on flow cytometric analyses of
picophytoplankton (PRO, Prochlorococcus; SYN, Synecho-
coccus; PEUK, picoeukaryotic algae) and biovolume-based
microscopical assessments of prymnesiophytes (PRYM),
Phaeocystis (PHAEO), diatoms (DIAT), and dinoflagellates
(DINO). Distributions are the means of three sampling dates
in ambient waters and 4 days of sampling during the peak of
the patch bloom. Inserts indicate that the instantaneous
growth rates (m) of all taxa shift up in response of added Fe,
but most size categories are maintained at constant levels by
corresponding increases in microzooplankton grazing (g),
except for >20 mm diatoms dominated by Pseudo-nitzschia.
(Modified from Landry et al. [2000b].)
16 of 24
can be relatively modest, e.g., a 50% increase in grazer
standing stock, or perhaps just slight increases in prey
vulnerability due to Fe-enhanced changes in cell size or
physiochemical cell surface properties [Monger and
Landry, 1990; Monger et al., 1999].
[47] Diatoms do not dominate Fe-stimulated blooms
because they physically cannot be eaten by microzooplank-
ton. Within this diverse group, there are clearly organisms
with appropriate size, behaviors and apparent preferences
for feeding on diatoms [e.g., Gaines and Taylor, 1984;
Jacobson and Anderson, 1986]. In IronEx-2, large dino-
flagellates and ciliates eventually exerted a heavy grazing
toll on Pseudo-nitzschia [Landry et al., 2000b], and large
protists were also the major grazers in the diatom-dominated
waters of SOFeX-South [Coale et al., 2004; M. Landry,
personal communication, 2005]. It does appear to be true,
however, that initially rare and relatively large diatoms
enjoy a release from heavy grazing pressure in at least the
early stages of an Fe-stimulated bloom because their spe-
cialized grazers are not sufficiently abundant to control
them when their growth rates are strongly stimulated by
the added Fe. The larger the difference between the growth
rates of large rare species in Fe-deficient ambient waters and
their maximal growth potential with added Fe, the larger
will be their net growth rate advantage in the early bloom. It
is also likely the case that regulatory potential by micro-
zooplankton grazers diminishes with increasing cell size of
phytoplankton, such that ‘‘giant’’ diatoms, at the extreme,
are minimally vulnerable to such losses. Thus grazing
pressure would seem to act in a way that systematically
reinforces the selective growth advantages of large cells
under Fe-replete conditions, accelerating, in fact, the rate at
which they can rise relative to other cells to dominate the
community response.
8. Carbon Fluxes
[48] Photosynthetic fixation of CO
in all experiments
depletes the pool of dissolved inorganic carbon (DIC) in
seawater by converting it into particulate organic carbon
(POC). The DIC loss is paralleled by a decrease of the
fugacity of CO
in surface waters (Figures 3, 4, 6, and 11),
where an undersaturation versus atmospheric CO
develop. For a sufficient rate of gas exchange, this under-
saturation may drive an influx of CO
from the air into the
sea, thus somewhat replenishing the DIC pool. In addition,
part of the POC inventory may settle out into deeper layers,
thus exporting carbon into the deep sea (Figures 8 and 9).
[49] A detailed comparison of carbon budgets among the
eight Fe experiments would be desirable, but the designs,
implementations, weather conditions and actual evolutions
of these experiments have been quite different. Patch
dilution has notably varied greatly (Figure 15) and efforts
to quantify this using the SF
He) tracer(s) have
proven quite challenging [Goldson, 2004; Bakker et al.,
2005; C. S. Law et al., Patch evolution and the biogeo-
chemical impact of entrainment during an iron fertilization
experiment in the subarctic Pacific, submitted to Deep-Sea
Research, Part II, 2005], if pursued at all. In general, the
variability and patch dilution interfere with sampling, for
example at any given day of any experiment nobody can
guarantee the true core (SF
maximum) of the patch was
sampled. In other words, the response reported is intrinsi-
cally a function of sampling strategy and intensity. Also
sampling grids differ between variables, the Primary Pro-
duction assay typically being done at one in-patch station,
while some state variables have been mapped extensively.
Figure 22. Depth-integrated primary production (green
bars (mmol m
)) compared with the depth-integrated
inventory change terms (mmol m
) of DIC loss (blue
bars), POC gain (orange bars), replenishment of CO
by air/
sea gas exchange (yellow bars), and loss by export (red
bars) of settling particles into deeper water layers. Primary
production values as measured inside the Fe-enriched
patches from a recent compilation [Coale, 2004]. Owing
to continuing primary production in ambient (out-patch)
waters, the primary production enhancement (PP
) solely due to Fe enrichment would be less (not
shown). The decrease of DIC is about half (average is 51%,
s.d. 26%) of the primary production, ranging from 16 to
87% in SOFeX-North and SEEDS, respectively. The
buildup of POC biomass is about one-quarter (average
26%, s.d. 21%) of primary production, ranging from 8 to
68% in SOFeX-North and SEEDS, respectively. In general,
both the air/sea exchange term and the export flux tend to be
small or negligible and difficult to quantify during the time
course (12–24 days) of the experiments. The CO
gas flux
into the sea averages at 3% (s.d. 1.7%) of primary
production, ranging from 1.2% in SOIREE to 5% in
SOFeX-South. Compared to the DIC decrease, the CO
flux into the sea averages at 8% (s.d. 5%), ranging from
2.7% in SOIREE to 13% in both SOFeX sites. The export
estimates range from virtually nil (hence not discernible in
graph) for SOIREE [Charette and Buesseler, 2000], to 3%
of primary production in SERIES, to 12% in both SEEDS
and SOFeX-South, and as high as 1027% in IronEx-2
(plotted is average 33 of 15 and 50 mmol m
; see text
[Bidigare et al., 1999]). Export of SEEDS indirectly from
budget [Tsuda et al., 2003, supplement]. Sources are as
follows: Steinberg et al. [1998]; Bidigare et al. [1999];
Tsuda et al. [2003]; Boyd et al. [2004a]; Coale et al.
[2004]; Buesseler et al. [2004]; Coale [2004]; Bozec et
al. [2005]; Bakker et al. [2005]; and U. Riebesell et al.
(unpublished manuscript, 2003).
17 of 24
Finally, the C budgeting efforts for various experiments
(sources as in caption Figure 22) have used different
approaches. Thus overall, the comparison presented here
is somewhat incompatible. Further study may improve this,
but full comparability may never be achieved.
[50] Depth-integrated rate estimates (mmol m
the different Fe fertilization experiments tend to vary less
(Figure 22) than previously shown maximum changes per
volume seawater (Figure 11). A deep WML is unfavorable
for phytoplankton growth, for example, but the effect is
partially offset by integrating over a greater depth. Thus the
‘‘rankings’’ of experimental impact shift somewhat between
Figures 11 and 22. On this basis, the primary production of
IronEx-2 now exceeds that of SEEDS. This is consistent
with the twofold higher optimal growth rates of IronEx-2
predicted from temperature differences (Figure 14).
[51] For the experimental data represented in Figure 22,
measured DIC drawdown averages half (51 ± 26%) of
primary production rates, from
C uptake measurements
which typically underestimate true gross production by a
factor of two or more [e.g., Laws et al., 2000]. In the same
data set, the POC increases average one quarter (26 ± 22%)
of primary production. Excluding the unusually high ratios
for SEEDS, these POC ratios reduce to 45% of DIC
drawdown and 18% of primary production. It is clear from
these relationships that only SEEDS demonstrated the kind
of response, very high efficiency in moving carbon from
DIC to POC pools via photosynthetic fixation, that one
might associate with a relatively pure phytoplankton
‘‘culture.’’ More generally, the transfers are characterized
by large inefficiencies (only 1826% of production accu-
mulates as POC), which speaks to the importance of loss
processes due to grazing and related trophic processes. Such
results are consistent with rate estimates of phytoplankton
instantaneous growth and biomass accumulation in the
fertilization experiments. For example, in IronEx-2, growth
rates of 1.5 to 2 cell doublings d
(mof 1.0–1.4 d
produced only a net fivefold increase in phytoplankton
carbon biomass over the course of a week [Landry et al.,
2000a]. Similarly, in the SOFeX-South patch, phytoplank-
ton biomass only doubled despite mean estimated growth
rates (mof 0.2–0.3 d
) that could have led to a biomass
increase of 20-fold or more [Coale et al., 2004; M. Landry,
personal communication, 2005]. Because production/bio-
mass accumulation precedes grazer responses, there must
also be a substantial time dependency to calculated esti-
mates of the DIC )primary production )POC transfer
ratios. For example, phytoplankton POC estimates pla-
teaued for 4–5 days at peak levels in the IronEx-2 patch,
during which phytoplankton continued to grow at a high
rate while their biomass remained static. Clearly, during
such times, in the mid to late stages of bloom response to
added Fe, the ratios of DIC and POC changes to time-
integrated primary production should decline significantly.
[52] Of the average 70 80% of primary production that
does not accumulate as POC in Fe-fertilized patches, some
appears as DOC or contributes to export. Reports on DOC
changes have been sporadic. In CARUSO/EisenEx over the
first 12 days, during which the DIC decreased 12 mmol m
(Figure 6), the DOC showed a small increasing trend from
about 48 to 52 mmol m
suggesting a net increase on the
order of 4 mmol m
30% of the DIC decrease. However
the DOC data were scattered, and over the complete 21 days
there was no real trend. In addition, the 4 mmol m
is hardly discernible at an about 1 mmol m
[53] The CO
gas flux into the sea has been calculated for
most experiments and is a small 8% portion of the DIC
removal rate, ranging from 2.7% at SOIREE to as much as
13% for both SOFeX sites (Figure 22). The gas flux tends to
be about 3% of primary production (Figure 22). The
percentage variability between experiments is partly real,
partly also due to different calculation approaches and
applied gas exchange coefficients [e.g., Wanninkhof, 1992;
Wanninkhof and McGillis, 1999]. Nevertheless, the slow
replenishment of CO
from the air is as expected due to the
slow relaxation time of this gas as a result of its equilibra-
tion reactions with the seawater, as opposed to nonreactive
gases, e.g., O
or SF
. On the other hand, this also implies
that CO
supply from the air continues long after the
observer ships have left the scene. Hence the overall
drawdown of CO
from the air likely is more then shown
here only for the 12–24 day observation periods of indi-
vidual experiments. In the end, the DIC deficiency (e.g.,
Figures 6 and 11) will be largely compensated for from the
atmosphere, as well as from net heterotrophic respiration,
once the bloom has collapsed. Such a collapse was observed
in SERIES, but the CO
gas flux results are not yet
available. The relative contribution of both terms (gas flux
versus respiration) will remain the subject of debate until
longer observation strategies are implemented in this type of
[54] Export flux of organic carbon into deeper waters has
been assessed by difference from budget calculations. For
SEEDS an elegant effort has been reported [Tsuda et al.,
2003, supplement]. Similarly for CARUSO/EisenEx (not
shown) such an effort has been made (U. Riebesell et al.,
unpublished manuscript, 2003). However with export being
only a small fraction of primary production and the changes
in DIC and POC, and given the difficulty in assessing DOC
and its changes, calculated export signals hardly exceed the
noise of the overall budget, if at all. The export of organic
matter remained constant in SOIREE, perhaps due to its
short duration and patch dilution [Charette and Buesseler,
2000; Nodder and Waite, 2001]. The most direct evidence
for export was observed in sediment traps of SERIES upon
collapse of the bloom (Figure 9 (bottom)). However, deri-
vation of an overall export number does require extra
information on, e.g., trapping efficiencies [Boyd et al.,
2004a]. Finally, for SOFeX-South, the observed
deficiencies have led to an estimate of carbon export which
is significant, yet still modest relative to similar estimates
for the natural Southern Ocean [Buesseler et al., 2004,
9. Light Climate Due to Wind Mixed Layer
[55] Nine experiments in the 1993–2004 era have each
been successful in following an Fe-enriched water mass and
observing a distinct impact, small or large. The combined
nine experiments have demonstrated that the depth of the
wind mixed layer (WML), in regulating light climate, is the
major factor controlling photosynthesis in the high-nutrient
18 of 24
low-chlorophyll regions of the ocean. This is not surprising.
Light climate with its various parameterizations (e.g., PAR,
WML depth, self-shading) has been recognized in every
oceanography textbook [e.g., Lalli and Parsons, 1993] as a
key control of photosynthesis. Moreover, for some of the Fe
enrichment experiments in HNLC regions, light effects have
been considered explicitly, such as WML depth and self-
shading in SOIREE [Boyd et al., 2000; Gall et al., 2001b],
and self-shading in SOFeX [Coale et al., 2004], and the
unfavorable WML depth during CARUSO/EisenEx [Bozec
et al., 2005]. Nevertheless it is by combination of these
experiments (Figure 12; Tables 2 and 3) that the dominant
role of WML depth for the worldwide HNLC regions has
become more evident. In other words, when challenged to
specify just one over-ruling limitation for each individual Fe
enrichment experiment, one might conclude from Figure 12
that SOIREE and CARUSO/EisenEx in the Southern Ocean
were predominantly light limited, while the SEEDS and
SERIES regions were predominantly Fe limited, but
IronEx-2 and SOFeX-South and SOFeX-North were inter-
mediate between limitation by light and iron. However, the
concept of one overruling limiting factor is fruitless [de Baar,
1994; de Baar and Boyd, 2000]. Instead colimitation by iron
and light [Sunda and Huntsman, 1997; van Leeuwe, 1997;
Maldonado et al., 1999; Lancelot et al., 2000; van Oijen,
2004] best describes the HNLC regions in 40% of the world
oceans. Otherwise, the case for predominantly Fe limitation
in SEEDS and SERIES is further underlined by the virtual
complete exhaustion of notably silicate as well as nitrate
(Figure 8 and Figure 10 (middle)) after 13 and 18 days
respectively, where during SERIES indeed the bloom was
observed to collapse in days 19–23 (Figure 10 (top)).
[56] The well-documented climatology of wind velocity
and WML depths in the world oceans [Monterey and
Levitus, 1997] (available at is a
major resource when one wishes to understand, predict or
simulate what prevents HNLC regions from achieving full
biomass growth potential. Notably in the Southern Ocean
this is the case [Mitchell et al., 1991; Lancelot et al., 1993,
2000; Hannon et al., 2001; Pasquer et al., 2005]. Here the
most favorable conditions are in austral summer months
December–January. Indeed SOFeX-South in January 2002
showed a major impact of Fe enrichment. These 2 months
being favorable also for many other lines of research and
expeditions, it has proven to be very difficult to secure
suitable shiptime for Fe experiments in the Southern Ocean.
Thus SOIREE had been accommodated during late summer,
and CARUSO/EisenEx during early austral spring, when
wind and WML conditions were not optimal for light.
10. Efficiency of Moles Carbon Removed per
Moles of Iron Added
[57] The key role of light climate also implies that simple
stoichiometric arguments for the amount of Fe required for a
given level of C, N, P or biogenic Si production by
Table 3. Preliminary Overview of Derived DIC/Fe Efficiencies for Several Experiments
Acronym Fe, kg Fe DIC Removal DIC
WML Depth, m Patch Size, m
DIC Loss,
DIC/Fe Efficiency,
IronEx-1 450 8058 moles 6 10
mol m
A 35 64,000,000 13,440,000 1668
IronEx-2 449 8039 moles 27 10
mol m
A 40 72,000,000 77,760,000 9672
Ironex-2 449 8039 moles 27 10
mol m
A120,000,000 129,600,000 16,120
SOIREE 1745 31,246 moles 400 t B65 33,302,806 1066
SOIREE 1745 31,246 moles 800 t B66,605,612 2132
SOIREE 1745 31,246 moles 1389 t C 115,643,993 3701
EisenEx 2340 41,900 moles 1433 t C 70 119,307,302 2847
SEEDS 4 10
mol m
61 10
mol m
see text 12.5 15,000
SEEDS 350 6267 moles 1.3 mol m
D80,000,000 104,000,000 16,595
SOFeX-North 1712 30,655 moles 14 10
mol m
D 45 225,000,000 126,000,000 4110
SOFeX-South 1260 22,561 moles 23 10
mol m
E 35 225,000,000 181,125,000 8028
SOFeX-South 1260 22,561 moles 23 10
mol m
E1,000,000,000 805,000,000 35,680
SERIES 489 41.3 10
mol m
DPP 1.61 mol m
F30 38,983
SERIES 489 41.3 10
mol m
DDIC 1.1 mol m
SERIES 489 8756 moles DPOC 1776 t F 147,864,458 16,887
SAntarctic 5345 95,708 moles 416,076,295 4347
Total 8795 157,483 moles 885,140,752 5620
The added Fe (kg) is accurately known (where 1 mole Fe is 55.847 g). Patch dilution hampers the accuracy of the calculation of overall DIC loss. The
DIC removal from several sources is processed with various approaches (not necessarily consistent among each other) listed below (A– F) to obtain DIC
loss (moles) for each experiment. The total DIC loss (moles) by addition, where alternative estimates (values in italic font) were ignored. The DIC/Fe
efficiency scales inversely with WML depth (excluding IronEx-1): DIC/Fe = 240.3WML + 18818 (linear, with R
= 0.73 for n= 7 data points), with
SERIES deviating above the line and two SOFeXs deviating below the line. The grand total overall DIC/Fe efficiency is 5620 and about threefold below
the optimum 15,000 calculated for SEEDS. The Antarctic summation of SOIREE, EisenEx, and SOFeX-South in high-silicate, high-nitrate Antarctic
waters yields an efficiency DIC/Fe = 4347 and hinges largely on the most robust estimates by Bakker et al. [2005]. For the time being, this may serve as the
state-of-the-art gross DIC removal estimate for austral spring-summer-early autumn season (October– February), e.g., when assessing the impact of the
approximately 10-fold extra atmospheric Fe dust input [Edwards et al., 1998] during the Last Glacial Maximum.
(A) Steinberg et al. [1998]; integrated using WML and patch size of Figures 11 and 15 for IronEx-1 initial patch size; for IronEx-2, both initial and final
patch size provide lower and upper limit of C/Fe efficiency, respectively. (B) Boyd et al. [2000]; providing an upper limit of 800 t from algal carbon
integration over 200 km
patch size and 400 t when assuming algal carbon follows SF
distribution. (C) Bakker et al. [2005] estimates for both SOIREE and
EisenEx based on covariance analysis with the SF
distributions, apparently the most robust DIC removal estimates available now. (D) Tsuda et al. [2003,
Figure S1]. (E) Hiscock et al. [2002]; see also text description of SOFeX and Figure 11. Integration over initial patch size is deemed to provide a lower limit
estimate of C/Fe. For example, the larger final patch size of 1000 km
as suggested by Buesseler et al. [2004] would increase the DIC/Fe efficiency
accordingly to a quite high ratio DIC/Fe = 35,680. (F) Boyd et al. [2004a, Table 2]. The change in particulate organic carbon (DPOC) estimate for the entire
patch is based on Chl asignal from Sea-viewing Wide Field-of-view Sensor (SeaWiFS) ocean color image [Boyd et al., 2004a, 2004b, suppl. Figure 3]
multiplied by C/Chl aratio = 80 in patch center at day 18 and WML depth of 25 m. This yields a C/Fe efficiency similar to SEEDS. The DDIC estimate and
the DPP for the iron-mediated increase in net primary production are both for the patch center only and yield quite high C/Fe efficiencies.
19 of 24
phytoplankton, as popular during the past 15 years, do not
hold in general. This is even more the case because the
added [Fe(II)] is rapidly lost via the formation of colloids,
and then into larger (>0.2 mm) particles. In other words, for
any amount of dissolved Fe(II) added, only a minor portion
of perhaps about 20% remains soluble and available for
direct uptake by phytoplankton. Part of the colloid portion
may, or may not, become indirectly available via photore-
duction [Rijkenberg et al., 2005], and part of the particulate
Fe may, or may not, again become available due to
dissolution and remineralization via grazing [Barbeau and
Moffett, 2000].
[58] In SEEDS, the most optimal and perhaps also most
straightforward experiment, one single Fe infusion, bringing
the initial total Fe to about 4 10
mol m
maximum DIC removal of 61 10
mol m
(Table 3).
Accordingly, each Fe atom removed 15,000 carbon atoms as
. Where in general the DIC removal was found to
be about half of the primary productivity (Figure 22), in
SEEDS it was 88% such that one expects a ratio C/Fe =
17,250 for diatom growth in SEEDS. The cellular Fe
content of plankton has long been a vexing question, but
the first direct measurements of Fe quotas of individual
plankton cells have recently been made by Twining et al.
[2004b] detecting Fe in single cells by synchrotron X-ray
radiation (Table 3). Within the Fe-enriched patch of SOFeX-
South, the reported ratio C/F e = 25,000 [Twining et al.,
2004b] is remarkably consistent with above expected
17,250 in SEEDS. The C/Fe = 25,000 is substantially
less than initial suggestions of oceanic phytoplankton
cellular Fe requirements as high as 500,000 on the basis
of the Fe
paradigm in EDTA-manipulated laboratory
cultures [Sunda et al., 1991]. The ratio C/Fe = 33,000
previously calculated from excess (i.e., biogenic) particu-
late Fe in the deep North Pacific [Martin et al., 1989]
would agree more closely, but may be fortuitous as deep
biogenic particles are not necessarily comparable with the
Fe/C of primary production. The ratio C/Fe derived from
dissolved Fe versus nitrate (C/Fe = 483,000) or versus O
(C/Fe = 384,000) in the nutricline of the North Pacific
[Martin et al., 1989; Martin, 1992] (discussed by de Baar
and de Jong [2001, p. 164]) is much higher, but again not
necessarily comparable with newly synthesized phyto-
plankton cells.
[59] In fact, the DIC/Fe ratio of 15,000 of SEEDS is a
maximum value, occurring during the early build up of
the bloom with more to be returned to DIC by hetero-
trophic respiration during the decline phase. For the sake
of argument, the general POC buildup is about half of
DIC removal (the other half is recycled by respiration),
but higher at 79% for SEEDS such that the maximum
POC/Fe efficiency of in situ Fe enrichment would be on
the order of C/Fe = 11,800, potentially an upper limit for
drawdown of CO
from the atmosphere. In fact, the
thus far observed net export flux is only a few percent
(Figure 22), this in keeping with a typical fratio in the
order of 1–10% of primary production for ocean plank-
ton blooms. The primary production in general being
about twice the DIC removal but 115% for SEEDS, this
implies 1.15–11.5% of DIC removal will eventually be
exported. Thus the ultimate efficiency of CO
from surface waters would be more on the order of 150
1500 C atom for each Fe added. For all other conditions with
a deeper WML, notably in the Southern Ocean, and in all
other experiments (Figure 11), the DIC/Fe efficiency would
be less than the upper limit C/Fe = 11,800, here derived from
[60] The major uncertainty in such overall DIC/Fe effi-
ciency estimate is due to the patch dilution somehow to be
taken into account when converting from maximum DIC
loss (mol m
) to overall DIC removal (moles) for the
overall experiment. Here the above estimate for SEEDS is
relatively robust as its patch dilution factor was only
threefold. Table 3 provides an account of overall DIC/Fe
efficiencies which indeed tend to be less than the above
derived optimum DIC/Fe = 15,000 ratio, but all suffering
greater or lesser uncertainty due to patch dilution. Never-
theless, the derived C/Fe efficiencies, being either better
or worse, also tend to scale inversely with WML depth
(Table 3, caption).
11. Iron Fertilization During the Last Glacial
Maximum and Anthropocene
[61] The implications of above DIC/Fe ratio values for
the last deglaciation (17,00011,000 y BP) as well as for
intentional Fe fertilization of the modern ocean have been
reported elsewhere (H. J. W. De Baar et al., Iron makes big
diatoms blooming, but cannot change carbon dioxide and
climate, submitted to Science, 2005, hereinafter referred to
as de Baar et al., submitted manuscript, 2005). Briefly,
during the Last Glacial Maximum (LGM) the Fe dust input
into the Antarctic region was 11-fold the modern dust flux
[Edwards et al., 1998]. Sometime after this dust flux
terminated, the atmospheric CO
has risen initially with
80 10
atm and eventually with 90 10
atm to the
preindustrial value of 280 10
atm [Petit et al., 1999;
Watson et al., 2000]. Taking the Antarctic summation of
SOIREE, EisenEx and SOFeX-South in high-silicate high-
nitrate Antarctic waters yields an efficiency DIC/Fe = 4347
(Table 3), which by assuming 20% export, yields an
export efficiency C/Fe = 870. This combined with a factor
10 in Fe dust flux, 30% wet deposition of which 14%
dissolves, and a 3 month austral summer growth season,
yields an Fe fertilization effect which can account for only
0.5% of the observed rise of atmospheric CO
. Taking a
more favorable export ratio C/Fe = 3257 after Buesseler
et al. [2004], the Fe effect would be higher, but still only
2 % of the observed rate of atmospheric CO
When also taking a more favorable overall mean 32%
dust dissolution (operational defined range is 9–89%
[Edwards and Sedwick, 2001]) instead of above 30% of
which 14% dissolves, the Fe effect might be as high as
15% of the observed CO
[62] Similarly extrapolation to the current anthropogenic
fossil fuel CO
emission rate of about 6.6 Petagram C yr
(0.55 10
mol C yr
) would lead to a required Fe
fertilization of 0.63 10
mol Fe yr
or 35 10
kg Fe yr
i.e., 35 million tons Fe yr
(de Baar et al., submitted
manuscript, 2005). This is 40-fold more Fe than originally
hypothesized (430,000 tons Fe to remove 3 PgC yr
[Martin, 1990]). Extrapolation of the most favorable C
export of C/Fe = 3257 for only SOFeX-South in austral
summer [Buesseler et al., 2004] would yield a lower required
20 of 24
Fe fertilization of 0.17 10
mol yr
or 9.4 10
kg yr
This is 9.4 million tons Fe yr
12. Artefacts
[63] One major reason for in situ enrichment experiments
was to independently verify bottle incubations, notably
with respect to perceived artefacts of the latter. One such
artefact, the control bottles also outgrowing the field
biomass (Figure 1) due to more favorable light climate in
deck incubators, has now been confirmed. Indeed, while
Fe addition is effective when light is optimal (Figures 11
and 17), added Fe has little effect when light conditions are
[64] The in situ experiments have their own artefacts as
well [Boyd et al., 2002]. Most notably, the 100-fold higher
Fe is a strong perturbation of Fe chemistry, the effects of
which on phytoplankton growth have yet to be understood.
Moreover, the rapid formation of Fe colloids is reason for
some caution when interpreting coagulation of particles and
export fluxes with approaches and concepts developed in
the unperturbed natural ocean. Briefly, freshly formed Fe
colloids are adhesive and reactive and may not necessarily
be inert versus coagulation of biogenic debris and scaveng-
ing processes of trace elements and isotopes. In fact, Fe
colloid formation is a standard method worldwide for
purifying natural fresh waters in the production of drinking
water. Obviously the applied levels are much higher, but
some effectiveness at the typical 3 5 nM concentrations of
in situ experiments is not necessarily ruled out.
[65] Another physical phenomenon to be considered is
patch dilution (Figure 15), which gives rise to the chemostat
effect [Abraham et al., 2000]. Patch dilution can be over-
come, in principle, by fertilizing very large patches vis-a`-vis
the expected shear stress and wind forcing, such that the
core of the patch will be unaltered and dilution only a
boundary effect. On the other hand, the patch sizes used
thus far, 80 or 225 km
, are perhaps of similar order as
natural wet deposition mesoscale events (combined rain/
dust storms) or natural upwelling events, bringing in extra
Fe from either above or below. In other words, patch
dilution is, on the one hand, an artefact for understanding
details of Fe responses in a controlled reproducible manner,
yet, on the other hand, perhaps quite realistic in the natural
13. Perspectives
[66] Experimental oceanography has now been proven a
powerful and exciting approach for unraveling the drivers
and inner mechanisms of plankton ecosystems. This pre-
liminary synthesis next needs more rigorous verification by
application of a generic plankton ecosystem simulation
model to most or all of the 8 9 experiments. This is crucial
also for the design of the next generation of experiments,
some by tinkering with innovative techniques for delivering
the extra Fe more naturally and effectively, others by relying
on natural Fe supply and gradients instead. Moreover one
would like to be able to follow an experimental water body
over longer time periods of several months. Finally new
techniques are desirable to quantify more reliably and
routinely the exchanges of CO
, DMS and other biogenic
gases with the atmosphere, as well the thus far difficult to
quantify biogenic export to the deep ocean.
[67]Acknowledgments. The authors are most grateful to the organ-
izers of The Ocean in a High CO
World symposium for the invitation, with
special thanks to Maria Hood for realizing an excellent and exciting
meeting within sight of the iron tower of Eiffel. During preparation the
team of coauthors kindly and diligently provided much data, graphics, and
other precious findings and insights, where the temptation for special thanks
to special coauthors is here avoided. Silvio Pantoja and two anonymous
referees are acknowledged for their constructive editorial comments as well
as patience. This and detailed comments by coauthor Paul Harrison have
remedied many flaws in the first submitted version. Hendrik van Aken,
Yvonnick Le Clainche, and Jaap van der Meer kindly assisted with various
data and graphics. The vision and enlightenment of the late John Martin as
founding father of this exciting research field cannot be overestimated. This
paper is dedicated to all the heroes who went out to sea to dump in the iron
and do the accurate measurements. Their original research articles are the
basis of this preliminary review. We are most grateful to the officers and
crew, and our shipboard fellow scientists, aboard the research vessels
Columbus Iselin,Melville,Tangaroa,Kaiyo-Maru,Revelle,John P. Tully,
and El Puma and icebreakers Polarstern and Polar Star. The commitment
and support of all these people, and the dedication of ships by AWI,
Fisheries Agency Japan, NIWA, the Canadian and U.S. Coast Guards, and
U.S. National Science Foundation Ocean Sciences, have created and
realized this new era of experimental oceanography. This research was
supported by the European Union through programs CARUSO (1998
2001), IRONAGES (1999 – 2003), and COMET (2000 – 2003); the Nether-
lands-Bremen Oceanography program NEBROC-1; and the Netherlands
Organization for Research NWO through the Netherlands Antarctic Pro-
gram project FePath. Both the U.S. National Science Foundation and the
U.S. Department of Energy provided significant support for the SOFeX
program. M.R.L. acknowledges the U.S. National Science Foundation for
support of IronEx and SOFeX projects and related studies (OCE-9912230,
-9911765, and -0322074).
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... The region investigated here presents two major hydrological fronts ( Fig. 1): the sub-Antarctic front (SAF) defined here as the isotherm 12 • C and the polar front (PF) defined by the isotherm 5.2 • C (the mean position of the fronts in January is deduced from temperature and salinity observations in surface and subsurface waters). South of the SAF, one finds generally HNLC conditions (high-nutrient low-chlorophyll; Minas and Minas, 1992) mainly due to iron limitation (Martin et al., 1990;de Baar et al., 2005). However, localised areas in the Southern Ocean offer a favourable environment for phytoplankton development notably due to the island mass effect that supplies micronutrients (iron) to the surface waters (e.g. ...
... For nutrients (nitrite, nitrate, silicate and, for some years, phosphate), samples were filtered (at 0.2 µm) and either poisoned with HgCl 2 and kept cold (for nitrite, nitrate and silicate) or frozen at −80 • C (for phosphate). Nitrite, nitrate and silicate were analysed on board or at LOCEAN by colorimetry using an auto-analyser (Bran + Luebbe) according to the method of Tréguer and Le Corre (1975) until 2009, then following the method of Coverly et al. (2009). The uncertainty of these measurements is on the order of ± 0.1 µmol kg −1 . ...
Full-text available
The decadal changes in the fugacity of CO2 (fCO2) and pH in surface waters are investigated in the southern Indian Ocean (45–57∘ S) using repeated summer observations, including measurements of fCO2, total alkalinity (AT) and total carbon (CT) collected over the period 1998–2019 in the frame of the French monitoring programme OISO (Océan Indien Service d'Observation). We used three datasets (underway fCO2, underway AT–CT and station AT–CT) to evaluate the trends of fCO2 and pH and their drivers, including the accumulation of anthropogenic CO2 (Cant). The study region is separated into six domains based on the frontal system and biogeochemical characteristics: (i) high-nutrient low-chlorophyll (HNLC) waters in the polar front zone (PFZ) and (ii) north part and (iii) south part of HNLC waters south of the polar front (PF), as well as the highly productive zones in fertilised waters near (iv) Crozet Island and (v) north and (vi) south of Kerguelen Island. Almost everywhere, we obtained similar trends in surface fCO2 and pH using the fCO2 or AT–CT datasets. Over the period 1998–2019, we observed an increase in surface fCO2 and a decrease in pH ranging from +1.0 to +4.0 µatm yr−1 and from −0.0015 to −0.0043 yr−1, respectively. South of the PF, the fCO2 trend is close to the atmospheric CO2 rise (+2.0 µatm yr−1), and the decrease in pH is in the range of the mean trend for the global ocean (around −0.0020 yr−1); these trends are driven by the warming of surface waters (up to +0.04 ∘C yr−1) and the increase in CT mainly due to the accumulation of Cant (around +0.6 µmol kg−1 yr−1). In the PFZ, our data show slower fCO2 and pH trends (around +1.3 µatm yr−1 and −0.0013 yr−1, respectively) associated with an increase in AT (around +0.4 µmol kg−1 yr−1) that limited the impact of a more rapid accumulation of Cant north of the PF (up to +1.1 µmol kg−1 yr−1). In the fertilised waters near Crozet and Kerguelen islands, fCO2 increased and pH decreased faster than in the other domains, between +2.2 and +4.0 µatm yr−1 and between −0.0023 and −0.0043 yr−1. The fastest trends of fCO2 and pH are found around Kerguelen Island north and south of the PF. These trends result from both a significant warming (up to +0.07 ∘C yr−1) and a rapid increase in CT (up to +1.4 µmol kg−1 yr−1) mainly explained by the uptake of Cant. Our data also show rapid changes in short periods and a relative stability of both fCO2 and pH in recent years at several locations both north and south of the PF, which leaves many open questions, notably the tipping point for the saturation state of carbonate minerals that remains highly uncertain. This highlights the need to maintain observations in the long-term in order to explore how the carbonate system will evolve in this region in the next decades.
... Primary production in large regions of the ocean is chronically limited by low Fe availability (Behrenfeld et al. 2009;Moore et al. 2013). Certain diatoms are particularly successful in these regions due to their low Fe requirement for growth (Maldonado and Price 1996;Price 2005;Quigg et al. 2003;Sunda and Huntsman 1995b) and their ability to capitalize on episodic Fe inputs (Ardyna et al. 2019;Blain et al. 2007;de Baar et al. 2005;Moore et al. 2007). ...
... Iron (Fe) plays an important role in many environmental processes, including marine primary production, and thereby affects the global carbon cycle (Boyd and Ellwood, 2010;Tagliabue et al., 2017). Specifically, Fe is an essential micronutrient for marine phytoplankton, and low dissolved Fe concentrations in seawater limit primary production in >30% of the surface ocean (de Baar, 2005;Hutchins and Bruland, 1998;Martin and Fitzwater, 1988;Morel et al., 1991). Iron sources to these so-called High Nutrient Low Chlorophyll (HNLC) ocean regions include inputs from atmospheric deposition, continental margin sediments and hydrothermal vents (Conway and John, 2014;Duce and Tindale, 1991;Lam and Bishop, 2008;Tagliabue et al., 2010). ...
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Atmospheric deposition is a key mode of iron (Fe) input to ocean regions where low concentrations of this micronutrient limit marine primary production. Various natural particles (e.g., mineral dust, volcanic ash) and anthropogenic particles (e.g., from industrial processes, biomass burning) can deliver Fe to the ocean, and assessment of their relative importance in supplying Fe to seawater requires knowledge of both their deposition flux and their Fe solubility (a proxy for Fe bioavailability). Iron isotope (⁵⁴Fe, ⁵⁶Fe, ⁵⁷Fe, ⁵⁸Fe) analysis is a potential tool for tracing natural and anthropogenic Fe inputs to the ocean. However, it remains uncertain how the distinct Fe isotopic signatures (δ⁵⁶Fe) of these particles may be modified by physicochemical processes (e.g., acidification, photochemistry, condensation-evaporation cycles) that are known to enhance Fe solubility during atmospheric transport. In this experimental study, we measure changes over time in both Fe solubility and δ⁵⁶Fe of a Tunisian soil dust and an Fe–Mn alloy factory industrial ash exposed under irradiation to a pH 2 solution containing oxalic acid, the most widespread organic complexing agent in cloud- and rainwater. The Fe released per unit surface area of the ash (∼1460 μg Fe m⁻²) is ∼40 times higher than that released by the dust after 60 min in solution. Isotopic fractionation is also observed, to a greater extent in the dust than the ash, in parallel with dissolution of the solid particles and driven by preferential release of ⁵⁴Fe into solution. After the initial release of ⁵⁴Fe, the re-adsorption of A-type Fe-oxalate ternary complexes on the most stable surface sites of the solid particles seems to impair the release of the heavier Fe isotopes, maintaining a relative enrichment in the light Fe isotope in solution over time. These findings provide new insights on Fe mobilisation and isotopic fractionation in mineral dust and industrial ash during atmospheric processing, with potential implications for ultimately improving the tracing of natural versus anthropogenic contributions of soluble Fe to the ocean.
... Dust fertilization experiments during stratification of the Mediterranean Sea have been proven to result in significant increases in chlorophyll a concentration and primary production (e.g., Ridame et al., 2014). It has been observed that in situ Fe fertilization, whether artificial or natural, results in blooms dominated by large diatoms, which are often rare in the standing microalgal community (De Baar et al., 2005). These include the members of the genera Fragilariopsis, Pseudo-nitzschia, and Chaetoceros, in particular. ...
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Atmospheric mineral dust deposition plays an important role in providing nutrients to marine ecosystems. In this study, the climatology of dust deposition in the Adriatic Sea area was determined for the first time based on Modern‐Era Retrospective Analysis for Research and Applications, version 2 reanalysis from 1989 to 2019. The annual cycle of deposition exhibits two maxima: a stronger maxima in March–April and a weaker maxima in November. Wet deposition is a dominant process with a relative contribution to overall deposition from 67.35% to 88.53%. Deposition hot spots are along the Montenegrin coast and Otrant. The average contribution of dust deposition events (DDEs) is 16.5% (60.2 dy yr⁻¹), with the strongest deposition during 1999–2009 and a positive trend in deposited mass during the study period. The effect of dust deposition on primary production is observed by a high level of oxygen saturation up to 250% (usually it is lower, up to 150%) in the stratified middle water layer (5–8 m) of the central Adriatic marine system (Rogoznica Lake) during an intense wet deposition episode. Such extreme values of oxygen saturation can be taken as an indication of biological activity related to an increase in phytoplankton abundance and activity, diatoms in particular.
... In contrast to the bacteria, distinct effects in phytoplankton species composition were found in response to the different Fe and Mn availabilities in both experiments. Similar to other experiments in HNLC waters 8,[40][41][42] , the Fe addition significantly enhanced Chla build-up in both experiments (Figs. 3, 4). As up to 23-24 atoms of Fe are needed in both photosystems (PSI and PSII) for a single copy of the electron transport chain, 80% of the cellular Fe is required for photosynthetic electron transport 13,15 . ...
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While it has been recently demonstrated that both iron (Fe) and manganese (Mn) control Southern Ocean (SO) plankton biomass, how in particular Mn governs phytoplankton species composition remains yet unclear. This study, for the first time, highlights the importance of Mn next to Fe for growth of two key SO phytoplankton groups at two locations in the Drake Passage (West and East). Even though the bulk parameter chlorophyll a indicated Fe availability as main driver of both phytoplankton assemblages, the flow cytometric and microscopic analysis revealed FeMn co-limitation of a key phytoplankton group at each location: at West the dominant diatom Fragilariopsis and one subgroup of picoeukaryotes, which numerically dominated the East community. Hence, the limitation by both Fe and Mn and their divergent requirements among phytoplankton species and groups can be a key factor for shaping SO phytoplankton community structure.
This work presents a new method for determining iron-porphyrin-like complexes (Fe-Py) based on Continuous Flow Analysis (CFA) with chemiluminescence detection and its application to natural waters in an estuarine environment. The involved reaction is founded on luminol oxidation by hydrogen peroxide in the presence of Fe-Py complexes at pH 13. The detection limit is 7.2 pM hemin equivalent, the linear range extends to 150 nM and precision of the method is 6.4% at 0.25 nM (n = 8). This new method's detection limit is 15 times lower than the previous analytical procedure of Vong et al. (2007), based on Flow Injection Analysis (FIA) and using different chemical conditions. Moreover, the presented method is fast (90s/analysis), involves a low consumption of reagents, a small sample volume, and simplified sample handling. The method was applied to natural samples collected along the temperate macrotidal Aulne estuary (Bay of Brest, France). Here, we report for the first time on the spatial distribution of the Fe-Py complex concentration (dissolved, reactive particulate) over the entire salinity gradient of a macrotidal temperate estuary. The Fe-Py concentrations in the riverine and marine end-members were 0.873 ± 0.007 nM (S = 0.92) and 0.010 ± 0.004 nM (S = 34.86), respectively. Between these two salinities, non-conservative behaviour was observed, with an increase in Fe-Py concentrations to 1.142 ± 0.031 nM at S = 5.2 corresponding to the Maximum Turbidity Zone (MTZ), followed by a strong removal of Fe-Py in the salinity range 5–20. Then, the Fe-Py concentrations decreased linearly during mixing processes, reaching picomolar levels towards the coastal waters. The estimated entering flux from the river equaled 240 ± 2 g.d⁻¹ whereas the net flux to coastal sea waters was 95 ± 10 g.d⁻¹ leading to a loss of ~60%. The estuarine system globally acts as a sink for Fe-Py complexes, probably due to the aggregation of Fe-Py complexes on particles, to flocculation and/or sedimentation.